Dictyocaulus viviparus: re-emerging or never been away?

doi:10.1016/S1471-4922(02)02317-6

Trends in Parasitology

Volume 18, Issue 8, 1 August 2002, Pages 329-332

https://doi.org/10.1016/S1471-4922(02)02317-6 Get rights and content

Abstract

For over 40 years a highly effective vaccine against the bovine lungworm has been commercially available. The use of it successfully reduced the number of outbreaks in calves. However, the past decade has seen a dramatic increase in lungworm outbreaks in adult cows in the UK. This might indicate that Dictyocaulus viviparus is re-emerging as a significant parasite in the dairy cattle industry. Much is still unknown, and here the most important aspects requiring urgent attention are put into perspective.

Section snippets

Vaccine improvement

McKeand [4] gave several disadvantages of the current irradiated larval vaccine. It does not produce a sterile immunity nor confers life-long protection in the absence of a natural booster. Furthermore, it is relatively unstable and this limits its use. Consequently, a more stable recombinant vaccine against D. viviparus, producing longer lasting immunity would be an improvement. This type of work is particularly pursued in the UK, with a number of interesting articles published during the

Serodiagnosis

Since the 1980s, developments in this area have been achieved mainly in The Netherlands and Germany 8., 9., 10., 11., 12.. Currently, there are two highly specific and sensitive assays available, an ELISA in The Netherlands [8] and a dipstick test in Germany [11]. The dipstick assay can be carried out on whole blood samples, giving a result within 90 mins. The major disadvantage of both assays is that adult infections are required before they test positive, hence infections are not detected

Insufficient development of immunity

In the 1960s, it was noticed that, for example by Michel et al. [15], in the absence of infection, cattle remain susceptible regardless of age. Hence, if lungworm infections are prevented or suppressed during calfhood, it is possible that adult cows attract lungworm disease if exposed. Therefore, with the advent of suppressive parasite control schemes in the 1980s, one of the major lines of research has been to study whether calves grazing on pastures known to be infested with infective larvae

Limitations of controlled field studies

One of the main drawbacks of most studies on the effect of parasite control on immunity development is that most, if not all, used severe challenge of calves to infective larvae while they were being subject to some control strategy. Some of the control strategies allow for some infection getting through in between treatments or for a short period after the treatment regime, resulting in strong immunity development. Furthermore, it has recently been shown that protection can develop even when

Quantifying and defining exposure and protection

Many infections in calves will start with just a few larvae on pasture, resulting in a small proportion of a herd (e.g. only one or two calves) attracting a low level of infection insufficient to cause disease in these animals. Lungworm is a very fecund parasite, and the resulting larval excretion will produce a rapid and dramatic increase in pasture infectivity. This will result in both auto-infection of the calves initially infected and in a primary infection of those not yet infected. The

Host responses and intraspecific parasite variability

Two important aspects should not be neglected. First, there is a huge variability between hosts in their response to infection. Part of this variability will undoubtedly be host genetic in origin. It was recently shown that some calves show high levels of total immunoglobulin (Ig) E following primary infection, whereas others do not. This appears to be related to protection against a challenge infection [7]. The protected animals with high levels of total IgE also showed detectable

Concluding remarks

It does not appear that D. viviparus is re-emerging as a parasite of veterinary importance. This parasite has never been away, but the incidence of outbreaks appears to shift from calves to adult cows. If, for farmers, this is the only result of all efforts on improving parasite control and understanding lungworm epidemiology, then it has been a pitiful achievement. However, much has to be learned. The rapidly advancing molecular techniques and proteomics have a lot to offer to improve our

Acknowledgements

Maarten Eysker is gratefully acknowledged for his as ever critical comments on the manuscript and the many discussions on Dictyocaulus viviparus. Three referees gave highly appreciated comments on an earlier draft of the paper. Literature references have necessarily been selective. Many may justifiably feel their work should have been included in the list, and to those I apologize.

References (31)

J.B. Matthews
Immunisation of cattle with recombinant acetylcholinesterase from Dictyocaulus viviparus and with adult worm ES products
Int. J. Parasitol.
(2001)
C.A. Scott
A longitudinal study of local and peripheral isotype/subclass antibodies in Dictyocaulus viviparus-infected calves
Vet. Immunol. Immunopathol.
(1996)
J.B.W.J. Cornelissen
Evaluation of an ELISA for the routine diagnosis of Dictyocaulus viviparus infections in cattle
Vet. Parasitol.
(1997)
T. Schnieder
A dipstick immunoassay using a recombinant antigen for the rapid diagnosis of bovine dictyocaulosis
Res. Vet. Sci.
(1993)
T. Schnieder
The diagnostic antigen encoded by gene fragment Dv3-14: a major sperm protein of Dictyocaulus viviparus
Int. J. Parasitol.
(1993)
J.S. Gilleard
Dictyocaulus viviparus: Surface antigens of the L3 cuticle and sheath
Exp. Parasitol.
(1995)
W.T.R. Grimshaw
Development of immunity to lungworm in vaccinated calves treated with an ivermectin sustained release bolus or an oxfendazole pulse release bolus at turnout
Vet. Parasitol.
(1996)
D.E. Jacobs
Interactions between chemoprophylaxis and immunity to bovine parasitic gastroenteritis and bronchitis: pilot studies using an oxfendazole pulse release bolus
Res. Vet. Sci.
(1987)
S.M. Taylor
Induction of protective immunity to Dictyocaulus viviparus in calves while under treatment with endectocides
Vet. Parasitol.
(2000)
J.F. Michel
Studies on resistance to Dictyocaulus viviparus. IV. The rate of acquisition of protective immunity in infection of D. Viviparus
J. Comp. Pathol.
(1962)

R.K. Bain et al.

Parenteral vaccination of calves against the cattle lungworm Dictyocaulus viviparus

Res. Vet. Sci.

(1988)

C. Epe

Differences in a ribosomal DNA sequence of lungworm species (Nematoda: Dictyocaulidae) from fallow deer, cattle, sheep and donkeys

Res. Vet. Sci.

(1997)

J. Höglund

ITS2 sequences of Dictyocaulus species from cattle, roe deer and moose in Sweden: molecular evidence for a new species

Int. J. Parasitol.

(1999)

J.B. Dame

Genetic structure of populations of Ostertagia ostertagi

Vet. Parasitol.

(1993)

W.F.H. Jarrett

The natural history of parasitic bronchitis with notes on prophylaxis and treatment

Vet. Rec.

(1957)

Cited by (59)

To treat or not to treat: diagnostic thresholds in subclinical helminth infections of cattle
2023, Trends in Parasitology
Helminth infections of cattle place significant burdens on livestock production and farm economic efficiency. Heavy infections are relatively easy to detect and treat with anthelmintics. However, subclinical infections have major but often hidden impacts on animals, necessitating more refined diagnostics to detect them and ideally inform farmers about the likely impact of anthelmintic treatment on animal and herd performance. Here, we review recent advances in diagnosing three major cattle helminth infections – gastrointestinal nematodes (GINs), liver flukes, and lungworms – and the search for subclinical infection thresholds to guide treatment decisions. Combining refined diagnostic thresholds with farm-specific information on grazing systems and animal history enables farmers to tailor helminth treatments to specific epidemiological circumstances, thereby limiting anthelmintic resistance (AR) and boosting agricultural efficiency and food security.
Predicting the unpredictable? A climate-based model of the timing of peak pasture infectivity for Dictyocaulus viviparus
2022, Veterinary Parasitology
Citation Excerpt :
However, immunity will not develop without exposure to the parasite. It is particularly important that replacement cattle develop sufficient opportunities to develop the protective acquired immune response (Ploeger et al., 2000; Ploeger, 2002). Moreover, repeated application of anthelmintics will increase the risk of anthelmintic resistance developing in both lungworm and gastrointestinal nematode and ectoparasite species.
Outbreaks of cattle lungworm disease (Dictyocaulus viviparus) are explosive and costly. The unpredictability of the disease often encourages farmers to apply blanket anthelmintic treatments to the herd, which impede the acquisition of immunity, increase the risk of drug resistance, and interfere with efforts to reduce anthelmintic use against ubiquitous gastrointestinal nematodes. Improving our understanding of the factors which lead to a high risk of infection with lungworm, (including climatic pressure), would support a more targeted management. We present GLOWORM-FL-DV, the first mathematical model of the free–living stages of D. viviparus. The ecology of D. viviparus is unique compared with other strongylid nematodes due to its relationship with Pilobilus spp. fungi, which enhance the transmission potential. The role of the fungi was therefore incorporated into the model framework, informed by laboratory observations of Pilobolus spp. development and sporulation. The thermal niche of D. viviparus was characterised based on published and laboratory observations. Mortality of parasitic larvae increased significantly below 0^oC, and larval development occurred above 1.4^oC, whereas the estimated minimum temperature for migration via Pilobolus spp. was 8.8^oC. Model predictions were compared with antibody levels in bulk milk tank samples collected at two-weekly intervals from eight dairy herds across Great Britain over two grazing seasons. The model predicted high levels of larval abundance on pasture 46 days (38–52 days) before a rise in antibody levels and 22–26 days before the onset of clinical signs. The model assesses the impact of climate and weather on lungworm larval availability at pasture and provides a framework for the development of a risk forecasting system. This could help to focus vigilance for clinical signs at high-risk times and facilitate the targeted use of anthelmintics to prevent outbreaks, in support of sustainable parasite control.
Lungworms in ruminants from Brazil: A retrospective epidemiological study over four decades
2021, Veterinary Parasitology: Regional Studies and Reports
Lungworms such as Dictyocaulus spp. in cattle and small ruminants, and Muellerius capillaris and Protostrongylus rufescens in small ruminants are important pathogens, causing respiratory disease in these livestock species. Despite their veterinary importance, lungworms of livestock have been poorly studied in certain regions of the world, including Brazil. Therefore, much of their epidemiology and economic impacts on production remain unknown. This article aims to provide a comprehensive overview of the historical and current data published on lungworm infection of domestic ruminants in Brazil. This review consisted of a comprehensive search of technical and scientific publications between January 1980 to December 2020, using online sources such as PubMed, Google Scholar and Scielo. Twenty-four articles published over the last 40 years reporting lungworms exclusively in cattle (n = 16), goats (n = 6) and sheep (n = 1) in Brazil were included. In addition, a study (n = 1) with both goats and sheep were also utilized. Overall, 12 studies were based only on post-mortem examination, five in the detection of specimens in fecal samples, and seven were based on fecal analysis followed by post-mortem examination. Out of all studies, 66.7% (n = 16) articles registered D. viviparus, 4.2% (n = 1) D. filaria, 8.3% (n = 2) P. rufescens, 16.7% (n = 4) M. capillaris, and 4.2% (n = 1) co-infection by D. filaria and M. capillaris. The existence of suitable environmental conditions, as well as intermediate and definitive hosts in Brazil contribute for the survival and development of these nematode species. The majority of the reports of lungworms originate from the Southern and Southeastern regions of the country, whose mild temperatures likely contribute to their occurrence. Finally, lungworms of ruminants have been reported over the past four decades in Brazil, but most of the information was obtained at post-mortem examination. Therefore, further studies to investigate epidemiological aspects in different hosts and regions of the country are needed.
Association between Dictyocaulus viviparus bulk tank milk antibody levels and farmer-reported lungworm outbreaks
2020, Veterinary Parasitology
The lungworm Dictyocaulus viviparus can have a major impact on bovine health and productivity. Enzyme-Linked Immunosorbent Assays (ELISA), based on a recombinant Major Sperm Protein (MSP), have been developed to detect D. viviparus-specific antibodies in bulk tank milk (BTM). The objectives of this study are to assess the association between BTM optical density ratio’s (ODR) and farmer-reported lungworm outbreaks based on the clinical sign “coughing” throughout the grazing season and to compare the sensitivity and specificity of two ELISAs under field conditions. The Hannover MSP-ELISA and the prototype Svanova MSP-ELISA were used for the detection of D. viviparus antibodies in BTM samples on 717 dairy farms during the 2018 grazing season. Assuming all herds to be truly lungworm infected, the results show that the Svanova ELISA had a lower sensitivity (40-65%) and specificity (75-90%) for the detection of D. viviparus infections in BTM compared to the Hannover ELISA, which had a sensitivity of 42% and 74% and specificity of 100% and 98% at a cut-off of 0.41 ODR and 0.25 ODR, respectively. Therefore, analyses of the associations between milk antibody levels and farmer-reported outbreaks during the 2018 and 2019 grazing season were assessed using the Hannover ELISA, on 717 and 634 farms, respectively. A positive association was found between a farmer-reported outbreak and having at least two consecutive positive BTM ODR’s at a cut-off of 0.41 in 2018 (Odds Ratio (OR) = 5.5) and 2019 (OR = 2.8). Furthermore, there was a significant association between a farmer-reported outbreak and having a positive BTM ODR in August (OR 2018 = 4.4; OR 2019 = 2.8) and October (OR 2018 = 3.7; OR 2019 = 1.8). On the farms with a farmer-reported outbreak and positive BTM samples, over half (2018 = 77%; 2019 = 57%) of the positive ODR’s were situated before the outbreak and 47% (2018) and 42% (2019) within 12 weeks before the outbreak. In conclusion, there is a positive association between farmer-reported outbreaks and the occurrence of a positive BTM sample at the cut-off of 0.41 ODR using the Hannover ELISA.
Diseases of the Respiratory System
2019, Large Animal Internal Medicine
Diagnosis of bovine dictyocaulosis by bronchoalveolar lavage technique: A comparative study using a Bayesian approach
2018, Preventive Veterinary Medicine
Bovine dictyocaulosis is a pulmonary parasitic disease present in temperate countries, with potential important clinical and economic impacts. The Baermann technique is routinely used despite its low sensitivity in adult cows. Recently developed serological tests seem to offer better sensitivity, but validations of these tests in field conditions are few. We aimed to study two non-previously evaluated diagnosis methods of dictyocaulosis based on bronchoalveolar lavage sampling (BAL), which allows finding lungworm stages in the lungs as well as determination of eosinophilia. We compared them to the Baermann technique and serological tests. As no gold standard was available, we performed a Bayesian analysis by the simultaneous use of latent class and mixture models. The study was carried out during the 2015 pasture season on 60 adult cows originating from 11 herds with clinical signs of dictyocaulosis, and 10 apparently healthy cows originating from the teaching herd of VetAgro Sup, in France. Prevalence of infection was highly variable among herds with clinical signs (10–90%). Despite a maximal specificity (100%), the sensitivity of parasitological methods was low (7.4% for the Baermann sedimentation and 24.7% for the examination of BAL fluids). Better results were observed with serology (Se = 74.9%, Sp = 85.5%) with an optimal cut-off value estimated at 0.397 for the optical density ratio. Even better results were obtained with the count of eosinophil in BAL (Se = 89.4%, Sp = 85.2%) with an optimal cut-off value estimated at 4.77% for the eosinophil proportion. The BAL is a relevant diagnostic method of dictyocaulosis for practitioners due to the opportunity to perform two analyses (direct parasitic research and the eosinophil count) and to its good sensitivity and specificity.

View all citing articles on Scopus

View full text

Trends in Parasitology

Research updateDictyocaulus viviparus: re-emerging or never been away?

Abstract

Section snippets

Vaccine improvement

Serodiagnosis

Insufficient development of immunity

Limitations of controlled field studies

Quantifying and defining exposure and protection

Host responses and intraspecific parasite variability

Concluding remarks

Acknowledgements

Int. J. Parasitol.

Vet. Immunol. Immunopathol.

Vet. Parasitol.

Res. Vet. Sci.

Int. J. Parasitol.

Exp. Parasitol.

Vet. Parasitol.

Res. Vet. Sci.

Vet. Parasitol.

J. Comp. Pathol.

Res. Vet. Sci.

Res. Vet. Sci.

Int. J. Parasitol.

Vet. Parasitol.

The natural history of parasitic bronchitis with notes on prophylaxis and treatment

Vet. Rec.

Research update
Dictyocaulus viviparus: re-emerging or never been away?