BSE/TSE--the present epidemiologic and diagnostic situation

In 1992, 1994 and 1997, first BSE cases were diagnosed among imported cattle. The first domestic BSE case in Germany was confirmed on 26 November 2000. Altogether 192 cases (7 cases in 2000, 125 cases in 2001 and 60 cases in 2002) were reported (at the date: 7. August 2002). Comparing the BSE situation in Germany with other European countries under consideration of the surveillance schemes applied, Germany has a similar BSE incidence based on 100,000 adult cattle as France and Spain but a higher incidence than neighboring countries like The Netherlands, Austria and Denmark. At present, on average 2,3 cases per week are confirmed in Germany. With respect to the age distribution of the BSE cases, about 84% of all domestic cases confirmed originated out of the years 1995 and 1996 with a accumulation in 1996 (about 53% of all cases). Single BSE cases with the years of birth 1990, 1991 and 1993 demonstrate, that the BSE agent is circulating among the German cattle population at least since the beginning of the nineties. Between 1985 und 7 August 2002, scrapie was diagnosed in 26 sheep flocks in Germany, but alone during the year 2002 (until 7 August 2002) 11 scrapie affected sheep flocks were discovered.     

Imported and indigenous BSE cases in Germany

Bovine spongiform encephalopathy (BSE) is a transmissible fatal neurodegenerative disease in cattle with an average incubation time of five years. The first BSE case in an indigenous cow was detected in Germany in November 2000. This was almost eight years after the huge BSE epidemic in the United Kingdom had peaked, and several years after many EU member states had seen their first BSE case. In the 1990s, BSE had been diagnosed in six imported animals in Germany. However, after the implementation of an active surveillance programme using BSE rapid testing systems, 399 indigenous German BSE cases have been found up to the end of July 2006. The birth cohorts of 1995-1997 contribute to the vast majority of the first 250 German cases that were diagnosed between 2000 and 2003. However, the most recent German BSE cases belong primarily to the birth cohorts 1998-2000 which is indicative of a recycling of BSE infectivity at that time. Moreover, there were two BSE cases in cattle born in spring 2001, i.e. after the meat and bone meal feed ban had come into effect on 2nd December 2000. In this article, we describe the dynamics of the German BSE epidemic and compare these data with those of other countries that observed larger numbers of cases.     

Contagious Bovine Pleuropneumonia in Tanzania: Current Status

CBPP reappeared in Arusha, Northern Tanzania in 1990, having been introduced from Kenya. The disease spread rapidly to Mara region through rustling of sick or infected animals. In November 1992, an unrelated outbreak occurred in Kagera, having spread from Southern Uganda. Up to the end of December 1994, the disease appeared to be confined to Kagera and Arusha. In January 1995, CBPP was observed in Morogoro region, south of the central railway line. Thereafter, the disease spread through western Tanzania. More recently, further disease has occurred in the Southern Highlands and Central regions. The contaminated area now stretches roughly between latitudes 1° and 9°S and longitudes 30° and 37°E, with a cattle population of about 10 million. The direct losses incurred as a result of animal mortality, and vaccination campaign and disease surveillance costs have been assessed at over US$11 million. Indirect losses resulting from chronic disease are much more difficult to assess but are believed to be even higher. Control of the disease has been through restricting animal movements and a mass vaccination campaign. Uncontrolled animal movement during transhumance, trade, cattle thefts and vaccination breakthroughs facilitated the spread of the disease.     

Animal-derived feedstuffs as possible vectors for bovine encephalopathy (BSE) in Germany. Part 2: Assessment of vector risk for compounded feed

Specific conditions and practices of cattle feeding in Germany have to be taken into account for assessing the risk of feed born transmission of bovine spongiform encephalopathy, especially regarding the situation before the year 2000 when specific directives were introduced for feed production. The present retrospective epidemiological study includes data on feed production and the estimated amount of animal derived feedstuffs for the production of compounded feed for cattle. Risk assessment was performed based on the 'reproduction rate' (R0), that is defined as the estimated number of infections resulting from the processing of brain and spinal cord of BSE affected cattle that is recycled to bovines via feed. Under the conditions as given in Germany until the year 2000 the reproduction rate of BSE via the inclusion of animal derived feedstuffs in compounded feed production for cattle was estimated to be 1.1. Thus, it can be expected that BSE could be reproduced in the system, but with comparatively low efficiency. The expected incidence of BSE should be considerably lower compared to the situation during the 90th in the UK, due to the markedly lower recycling rate of animal protein in cattle feeding. Animal fat could have been a significant factor for BSE transmission due to contamination by proteinaceous brain and spinal cord material during the production process. The relative significance of fat containing feedstuffs for BSE transmission could have been higher in Germany compared to the situation in the UK where meat and bone meal was produced under different conditions and frequently used in higher proportions as an ingredient for compounded feed for ruminants.     

Model calculation to explain the BSE-incidence in Germany

The future development of BSE-incidence in Germany is investigated using a simple epidemiological model calculation. Starting point is the development of the incidence of confirmed suspect BSE-cases in Great Britain since 1988, the hitherto known mechanisms of transmission and the measures taken to decrease the risk of transmission as well as the development of the BSE-incidence in Germany obtained from active post mortem laboratory testing of all cattle older then 24 months. The risk of transmission is characterized by the reproduction ratio of the disease. There is a shift in time between the risk of BSE transmission and the BSE incidence caused by the incubation time of more than 4 years. The observed decrease of the incidence in Germany from 2001 to 2003 is not a consequence of the measures taken at the end of 2000 to contain the disease. It can rather be explained by an import of BSE contaminated products from countries with a high BSE incidence in the years 1995/96 being used in calf feeding in Germany. From the future course of the BSE-incidence in Germany after 2003 a quantification of the recycling rate of BSE-infected material within Germany before the end of 2000 will be possible by use of the proposed model if the active surveillance is continued.     

Updated prediction for the BSE epidemic in dairy cattle in Japan

Following the detection of the first case of Bovine spongiform encephalopathy (BSE) in Japan in September 2001, nine million cattle were tested for BSE up to the end of 2008. As a result, a further 28 cases were detected in dairy cattle. Using the mathematical model previously developed and surveillance data up to the end of 2008, we estimated the prevalence of BSE-infected animals within each birth cohort for the years 1995–2001. We predicted historic and future trends in the number of BSE-infected animals to be culled and anticipated BSE cases from each birth cohort. The results indicate that more infected animals (428 (95% CI: 59–727)) than previously estimated would have been culled from 1995 to 2001, and more cases (53 (95% CI: 25–101)) than previously predicted would have been detected during this period with a higher peak in 2001, if a BSE surveillance program as comprehensive as the present one was applied. In and after 2009, 0–2 cases of BSE would likely to be detected. As previously predicted, the BSE epidemic should be eradicated by 2012.     

BSE--present and future legal requirements

After BSE had first been recorded in November 2000 in a bovine animal born in Germany, national measures had immediately been taken and a great number of decisions taken at Community level resulting in substantial risk minimization. On 1 July 2001, Regulation No. 999/2001/EC came into force compiling all protection measures against BSE under Community law, including supplementary transitional measures. On the basis of the current legal situation, the evolving further development of key protection measures is described in the following.     

Animal feeding and feed legislation after the detection of the first indigenous BSE cases in Germany

In Great Britain, even the earliest tangible signs indicating the epidemiologic significance of meat and bone meal in the spreading of BSE soon gave rise to increasingly rigorous legislative measures regulating animal feedstuffs. In 1994 a ban on the feeding of animal proteins to ruminants was implemented throughout the entire EU. But until the first BSE cases were actually confirmed in locally raised cattle (November 2000), feeding practice and legislation more or less in Germany remained unaffected by the efforts undertaken in Great Britain. This situation was suddenly changed on 1 December, 2000, when the so-called "Verfütterungsverbot" was put into effect, a law which drastically extended bans regarding the feedstuffs (including fishmeal and animal fats) as well as the species concerned (all animals used in food production). In 2001 the "contamination" phenomenon (ingredients of animal origin were detected in mixed feeds) became a vital issue for the feed industry; through the media, the subject "feedstuff safety" gained a previously unseen level of public awareness. Those circles concerned with mixed feed production and animal husbandry were increasingly confronted with the consequences of the "Verfütterungsverbot" (availability and pricing of substitute ingredients; the demand for amino acids and inorganic sources of phosphorus; problems finding adequate substitutes for animal fats; poor digestibility of alternative components such as indigenous legumes or vegetable fats in calf diets; lower utilization rate of original phosphorus in mixed feeds with negative consequences for skeletal development). With the conditional approval of fishmeal (except in feeds for ruminants) the situation has eased again to a certain degree; on the EU level there are increasing signals pointing toward a political intention to reinstate the utilization of by-products of slaughtered animals qualified for human consumption (with the exception of fallen/dead animals and specific risk material) in poultry and swine feeding. In Germany, at least, the question of animal fat utilization for food-producing animals is still unsolved.     

The clinical diagnosis of BSE

Diagnosis of Bovine spongiform encephalopathy (BSE) is confirmed by specified laboratory methods on brain material. On the other hand clinical signs of manifest BSE are quite obvious. The first part of this paper describes case histories, clinical signs, laboratory findings and the most common differential diagnoses. On the basis of the data of actual prevalence in Germany, the role of clinical examination in eradication of BSE is dealt in the second part. Clinical diagnosis is a very sensitive and specific method when there is a high prevalence. According to the data from December 2000 to November 2001 prevalence in Germany was beyond 1 BSE case per 100,000 cattle or 3 cases per 100,000 cows. This very low prevalence decreases rapidly sensitivity and specificity of the diagnosis made by clinical examination. Therefore the main focus of field-diagnostics has to be laid on specified laboratory diagnostic methods. On the other hand prevalence of BSE-positive cattle is distinctly higher in the group of animals slaughtered in cases of illness or emergency than in cattle slaughtered on the regulatory bases. Nevertheless every veterinary practitioner should be aware of the clinical picture of BSE, clinical examination-routine and differential diagnosis, because occurrence of BSE is still possible in any dairy herd. At the moment it is not possible to make any statement if eradication of BSE can be reached in future.     

A model (BSurvE) for evaluating national surveillance programs for bovine spongiform encephalopathy

Our BSurvE spreadsheet model estimates the BSE prevalence in a national cattle population, and can be used to evaluate and compare alternative strategies for a national surveillance program. Each individual surveillance test has a point value (based on demographic and epidemiological information) that reflects the likelihood of detecting BSE in an animal of a given age leaving the population via the stated surveillance stream. A target sum point value for the country is calculated according to a user-defined design prevalence and confidence level, the number of cases detected in animals born after the selected starting date and the national adult-herd size. Surveillance tests carried out on different sub-populations of animals are ranked according to the number of points gained per unit cost, and the results can be used in designing alternative surveillance programs.     

Ten years of BSE surveillance in Italy: neuropathological findings in clinically suspected cases

Between 2001 and 2010, 244 clinically suspected cases of bovine spongiform encephalopathy (BSE) were reported in Italy. This report summarizes the neuropathological findings in cattle displaying clinical signs consistent with a diagnosis of BSE. All animal specimens were submitted for confirmatory testing; samples testing negative underwent neuropathological examination to establish the differential diagnosis. Immunohistochemistry for scrapie prion protein (PrPSc) at the level of frontal cortex was carried out to exclude atypical BSE. Neuropathological changes were detected in 34.9% of cases; no histological lesions were found in 52.3% of subjects; 12.8% of samples were found unsuitable for analysis. BSE was detected in one case, but no cases of atypical BSE were observed. This study identified the diseases most commonly encountered in the differential diagnosis of BSE; furthermore, it demonstrated that the surveillance system is necessary for monitoring neuropathological disease in cattle and for the detection of BSE cases.     

Factors affecting costs for on-farm control of salmonella in Swedish dairy herds

Background

The Swedish control program for salmonella includes restrictions and on-farm control measures when salmonella is detected in a herd. Required control measures are subsidised by the government. This provides an opportunity to study costs for on-farm salmonella control. The aim of this study was to describe the costs for on-farm salmonella control in Swedish cattle herds and to investigate the effects of herd factors on these costs in dairy herds.

Results

During the 15 years studied there had been a total of 124 restriction periods in 118 cattle herds; 89 dairy herds, 28 specialised fattening herds and three suckler herds. The average costs per herd for on-farm salmonella control was 4.60 million SEK with a median of 1.06 million SEK corresponding to approximately 490 000 and 110 000 EUR. The range was 0.01 to 41 million SEK corresponding to 1080 EUR to 4.44 million EUR per farm. The costs cover measures required in herd-specific control plans, generally measures improving herd hygiene. A mixed linear model was used to investigate associations between herd factors and costs for on-farm salmonella control in dairy herds. Herd size and length of the restriction period were both significantly associated with costs for on-farm control of salmonella with larger herds and longer periods of restrictions leading to higher costs. Serotype detected and administrative changes in the Swedish Board of Agriculture aiming at reducing costs were not associated with costs for on-farm salmonella control.

Conclusions

On-farm control of salmonella in Swedish cattle herds incurred high costs but the costs also varied largely between herds. Larger herds and longer restriction periods increased the costs for on-farm control of salmonella in Swedish dairy herds. This causes concern for future costs for the Swedish salmonella control program as herd sizes are increasing.     

Potential Risk Factors Associated with Bovine Spongiform Encephalopathy in Cattle from Schleswig‐Holstein,Germany

Since the first detection of bovine spongiform encephalopathy (BSE) in homebred cattle in Germany on 26 November 2000, 382 cases have been confirmed until 30 September 2005. Thirty‐two of these cases were reported from the Federal State of Schleswig‐Holstein (SH). There are hypotheses on the routes of infection for German cattle, but only few efforts have been made to assess potential risk factors by epidemiological studies. The purpose of this study was to identify potential risk factors at the farm level for the occurrence of BSE in cattle in SH. By applying the method of indirect standardization, the prevalence of various structural and management parameters of BSE‐affected farms in SH was compared with the prevalence of these parameters in a standard population of cattle farms from SH. The data describing the standard population were obtained by a cross‐sectional study performed in SH in 2003. Data of the BSE case population were available from the central German BSE case database. A possible association of the occurrence of BSE with the feeding of milk replacers to calves was observed. There was a clear indication that the occurrence of BSE was associated with the presence of pigs and/or poultry on the farm. This finding suggests that cross‐contamination of feed or cross‐exposition may have occurred in SH. The results obtained using the indirect standardization analysis were validated by multiple logistic regression. This study indicates that the feedborne path has been the principal route of transmission for the BSE agent in SH.     

Potential risk factors associated with bovine spongiform encephalopathy in cattle from Schleswig-Holstein, Germany

Since the first detection of bovine spongiform encephalopathy (BSE) in homebred cattle in Germany on 26 November 2000, 382 cases have been confirmed until 30 September 2005. Thirty-two of these cases were reported from the Federal State of Schleswig-Holstein (SH). There are hypotheses on the routes of infection for German cattle, but only few efforts have been made to assess potential risk factors by epidemiological studies. The purpose of this study was to identify potential risk factors at the farm level for the occurrence of BSE in cattle in SH. By applying the method of indirect standardization, the prevalence of various structural and management parameters of BSE-affected farms in SH was compared with the prevalence of these parameters in a standard population of cattle farms from SH. The data describing the standard population were obtained by a cross-sectional study performed in SH in 2003. Data of the BSE case population were available from the central German BSE case database. A possible association of the occurrence of BSE with the feeding of milk replacers to calves was observed. There was a clear indication that the occurrence of BSE was associated with the presence of pigs and/or poultry on the farm. This finding suggests that cross-contamination of feed or cross-exposition may have occurred in SH. The results obtained using the indirect standardization analysis were validated by multiple logistic regression. This study indicates that the feedborne path has been the principal route of transmission for the BSE agent in SH.     

The unrecognised French BSE epidemic

In France, implementation of systematic screening programs in 2000, as a complement to the mandatory reporting of animals with clinical signs of BSE (passive surveillance), revealed certain limitations of the mandatory system. Indeed, systematic screening showed that some BSE cases were not detected by the clinical surveillance system, implying considerable BSE case under-reporting throughout the epidemic. As the most likely explanation for variant Creutzfeldt-Jakob disease (vCJD) is exposure to the aetiologic agent of BSE, it is essential to reconstruct the French BSE epidemic pattern accounting for this under-reporting. We estimated age- and year-specific incidence rates of BSE by using a back-calculation method. This approach relies on the principle that the number of clinical BSE cases is the consequence of the number of BSE-infected animals after a known incubation time, defined as the time between infection and clinical onset. We generalized this model to take into account epidemiological characteristics of BSE, such as French cattle mortality, BSE case reporting probability, and age-dependent susceptibility and/or exposure to the BSE agent. We confirmed that the average BSE incubation period is five years and that the peak risk of bovine infection occurs between 6 and 12 months of age. The results also showed that the proportion of underreporting is the most influential parameter in the model, and that BSE was substantially underreported until rapid tests were introduced. Indeed, only 103 BSE cases were detected by passive surveillance up to June 2000, while we estimated that there was 301 200 (95% confidence interval (CI) [27 600-837 600]) cattle infected by the BSE agent. Despite uncertainty over the beginning of the epidemic, we showed that the French BSE epidemic in the late 1980s was completely undetected, and only the second wave, after 1990, was observed.     

How the surveillance system may bias the results of analytical epidemiological studies on BSE: prevalence among dairy versus beef suckler cattle breeds in France

Until recently, epidemiological studies on Bovine Spongiform Encephalopathy (BSE) were based on Mandatory Reporting Systems (MRS) of clinically suspect bovines only, but rapid diagnostic tests were validated in 1999 and are used for targeted surveillance in Switzerland, France and other countries, as a complementary and secondary tool. Data on 30491 cattle issued from a French pilot program targeted at cattle having died on the farm, subjected to euthanasia or sent for emergency slaughter, did not show any significant difference in BSE risk between dairy and beef suckler breeds. The data also revealed that part of the clinical cases of BSE escaped the MRS, which permitted to detect more dairy than beef suckler affected cattle compared to the targeted surveillance in the same period (from August to December 2000) and region (Bretagne, Pays de la Loire and Basse Normandie regions). Analyzing together the data of the targeted surveillance and mandatory reporting system programs with a non-conditional logistic regression, we found that the odds of a dead cow being a BSE case among all dead cattle was 3.2 times higher for dairy breeds compared to beef suckler breeds. This confirmed British findings but points out to the fact that considering either MRS or targeted surveillance data alone may possibly create biases in epidemiological studies on BSE.     

Temporal and spatial patterns of the clinical surveillance of BSE in France,analysed from January 1991 to May 2002 through a vigilance index

Between 1991 and mid 2000, the surveillance of Bovine Spongiform Encephalopathy (BSE) in France was based solely on clinical surveillance through a Mandatory Reporting System. Since 2000, the implementation of active surveillance programmes using rapid tests, as a complementary tool targeted at dead and slaughtered cattle has shown that part of the BSE cases were not detected with the clinical surveillance. In order to obtain a better knowledge of the strength of the clinical surveillance, we analysed a vigilance index defined as the ratio of negative clinical suspicions to the cattle population in the region and period of interest. The temporal analysis of the vigilance index showed that it did not vary much between 1991 and 1999, increased sharply since 2000, and then decreased partly in 2001. The geographical analysis of the variations of the vigilance index was performed at the department level by comparing the observed number of negative clinical suspicions per department to the expected number, computed on the basis of the national average index and standardised on the production type of the cattle - dairy versus beef suckling cattle. As assumed, the data followed a Poisson distribution. We observed a high geographical variation of the vigilance index: ten departments out of 91 presented a significantly higher vigilance index than the national one, and four a significantly lower vigilance index. The vigilance index showed that the clinical surveillance was heterogeneous during the past twelve years, both in time and geographic location, in a range of one to ten. So the apparent trend in the BSE epidemic during this period as well as the differences in the spatial incidence of BSE have to be analysed with caution.     

Review on the epidemiology and dynamics of BSE epidemics

The paper describes how the comprehensive surveillance of bovine spongiform encephalopathy (BSE) and studies carried out on these data has enhanced our knowledge of the epidemiology of BSE. Around 7, 000 BSE cases were detected through the screening of about 50 million cattle with rapid tests in Europe. It confirmed that the clinical surveillance had a poor capacity to detect cases, and also showed the discrepancy of this passive surveillance efficiency between regions and production types (dairy/beef). Other risk factors for BSE were being in a dairy herd (three times more than beef), having a young age at first calving (for dairy cattle), being autumn-born (dairy and beef), and being in a herd with a very high milk yield. These findings focus the risk on the feeding regimen of calves/heifers. Several epidemiological studies across countries suggest that the feedborne source related to meat and bone meal (MBM) is the only substantiated route of infection - even after the feed ban -, while it is not possible to exclude maternal transmission or milk replacers as a source of some infections. In most European countries, the average age of the cases is increasing over time and the prevalence decreasing, which reflects the effectiveness of control measures. Consistent results on the trend of the epidemic were obtained using back-calculation modelling, the R(0) approach and Age-Period-Cohort models. Furthermore, active surveillance also resulted in the finding of atypical cases. These are distinct from previously found BSE and classified in two different forms based on biochemical characteristics; their prevalence is very low (36 cases up to 1st September 2007), affected animals were old and some of them displayed clinical signs. The origin and possibility of natural transmission is unknown.     

Risk of introduction of BSE into Sweden by import of cattle from the United Kingdom

All cattle of United Kingdom origin imported to Sweden since 1980 were traced (n=94) and the probability that none of these imported cattle had clinical signs of bovine spongiform encephalopathy (BSE) at the year of slaughter (death) was calculated. If BSE had been introduced by live-animal imports, the consequences of such an event also was evaluated. The potential of the recently introduced surveillance system of high-risk cattle to detect such an event also was evaluated.We found that BSE most probably has not been introduced to Sweden by live-animal imports. We also found that, if this event had occurred and assuming a worst-case scenario that the animal was not prevented from being rendered, the rendering system (during certain periods) would not have prevented further spread of infection. Finally, we found that the BSE surveillance of high-risk cattle has not been in place long enough to verify that this event has not occurred (as of December 2001).