Contagious bovine pleuropneumonia: Possible future strategies for the control
of the disease in the PACE region

Gavin Thompson

PACE Programme, AU-IBAR, PO Box 30786, Nairobi, Kenya.

Background

Contagious bovine pleuropneumonia (CBPP) is a disease of cattle caused by Mycoplasma mycoides subspecies mycoides (small colony) (Mmm SC). It has occurred at one time or another in all regions of the world with the exception of South America and Madagascar (Schneider et al., 1994). It remains a significant constraint to cattle production in most of sub-Saharan Africa although a number of southern African countries have been free from the disease for many decades. Annual losses of US$ 2 billion have been ascribed to the disease in Africa although the reliability of this figure is uncertain (Masiga et al., 1999).

The disease is transmitted by direct contact between infected and susceptible individuals. When first introduced into a fully susceptible cattle population CBPP usually results in widespread mortality. For that reason it is included in the Office International des Epizooties (OIE) list A of diseases (OIE, 2003). As an example of the devastation it can cause, within two years of its introduction into South Africa in 1853 it resulted in the deaths of over 100 000 cattle and was a major contributor to the Great Xhosa Cattle-killing Movement of 1856 to 1857 which resulted in the starvation of tens of thousands of Xhosa people and the devastation of that nation (Henning, 1956; Peires, 1989). In endemic situations the disease has a variable course and is often insidious in nature. Clinical forms of the disease include peracute, acute and chronic. There are also cases of inapparent infection when clinical disease does not occur. The latter condition includes carriers (apparently healthy animals that have recovered from the disease) with encapsulated sequestra in the lungs containing live organisms. The extent to which carriers (also referred to as “lungers”) are important in the maintenance and spread of the infection is a matter of contention (Mariner, 2003).

The disease is difficult to reproduce in the laboratory and the study of its epidemiology is problematic in endemic situations because of the insidious nature of the disease. As a result, many aspects of the basic biology, epidemiology, immunology and pathogenesis of CBPP are poorly understood. In particular, determination of fundamental epidemiological parameters such as the basic reproductive number (R₀) that enable inferences to be drawn on factors such as herd immunity levels required to control the disease effectively, have only recently begun to be addressed (Mariner, 2003).

Historically, CBPP was a disease of Europe, the Americas and Asia but was eradicated from the United States, Canada and most of Europe in the 19^th Century through clinical diagnosis, movement control and slaughter of suspected cases (Provost et al., 1987). Although CBPP was present in sub-Saharan Africa prior to the colonial era, it was imported by ship into the southern-most part of the continent from Europe in the mid 19^th Century, as mentioned above, and subsequently spread as far north as Angola were it has persisted to the present (Windsor, 2000). The complexity of the origins of the infection in Africa is borne out by recent molecular epidemiological studies that have demonstrated three distinct African lineages of CBPP (Lorenzon et al., 2003).

Progress was made in controlling CBPP in Africa during the colonial era and first two decades following independence. Large parts of Southern, Western and Eastern Africa were cleared using slaughter and movement control (Hammond and Branagan, 1965), which later incorporated testing strategies based on the complement fixation test (CFT) (Campbell and Turner, 1936; Campbell and Turner, 1953; Huddart, 1960). However, a problem has been that the CFT, as well as the more recently developed competitive ELISA, are unable to detect carrier animals or those in the relatively long incubation period efficiently. Furthermore, lack of sensitivity on the part of these tests means that they can only be used to detect infected herds and are not reliable as a means of establishing freedom from infection in individual animals.

As vaccines became available, control programmes increasingly relied upon vaccination combined with movement control. However, vaccine coverage in Central, Eastern and Western Africa has declined since the closure of the Pan-African Rinderpest Campaign (PARC) in 1999 because during PARC vaccines against both rinderpest and CBPP were routinely administered to cattle in Central, Eastern and Western Africa (Kebkiba, 2003). In addition, it appears that the quality of vaccines used in recent times has declined (Waite and March, 2001). There are a number of factors that have contributed to this situation. Lack of independent quality control in some manufacturing facilities in Africa remains a problem and improper handling of the vaccine in the field (poorly maintained coldchains, for example) have resulted in sub-optimal quantities of vaccine strain mycoplasmas being administered to cattle (Thiaucourt et al., 2003). Occurrence of post-vaccination reactions in as many as 1% of vaccinated animals in some instances, as well as occasional deaths, have contributed to owner reluctance to use existing vaccines in certain areas. Furthermore, available serological tests do not detect vaccinated animals effectively so that sero-monitoring as a means of monitoring vaccination cover and establishing levels of herd immunity resulting from vaccination cannot be conducted effectively (Thiacourt et al., 2003).

In the 1980s and 1990s, economic crises afflicted many African countries and the subsequent structural adjustment programmes resulted in a decline in the funding of public veterinary services. This had an inevitable effect on surveillance and control programmes in Africa, including those for CBPP (Windsor, 2000). Other factors such as increasing public empowerment, recognition of the negative effects of movement control on pastoral livelihoods and a decline in the ability of veterinary services to enforce policies has decreased the effectiveness of measures adopted against CBPP. As a result, the disease is again present throughout most of Eastern, Central and Western Africa (Masiga and Domenech, 1995). The East African focus has advanced south into Tanzania (Bölske et al. 1995) and subsequently spread to most regions of that country. This poses a threat to northeastern Zambia. The long-standing focus in Angola has again invaded western Zambia and more recently still has spread to north-western Zambia. Furthermore, at least 12 African countries are engaged in or recovering from major internal conflict. These events involve mass movement of people and animals and constitute a significant factor in the spread of CBPP.

As indicated above, African governments are facing acute economic and financial problems that have affected their ability to fund programs of national or regional importance in the animal health field. Livestock and animal health budgets are already small and are being cut further. Most governments rely heavily on complementary donor funding from bilateral and multilateral partners to finance animal disease control programs. The sustainability of these programmes is therefore in doubt. Conversely, senior animal health officials of most African countries express the imperative for introducing an integrated regional programme to either eradicate the disease or to greatly lessen its impact on livestock producers (Reports of PACE workshops on CBPP; Addis Ababa, November 2001; Accra, February 2003). In the light of these two incompatible trends a question that needs to be answered is: As national financial resources are limited and declining in absolute and relative terms, how would an integrated regional programme be financed? In this regard it is necessary not only to establish the cost but also the return on such investment. For example, would investing, say, US$150 million in regional CBPP control over a 5 year period provide a better return than investing that money in human health improvement, education or infra-structure development?

Current policy advocated by PACE and AU-IBAR

In the final report of the Pan-African Rinderpest Campaign (PARC) the recommendation was made that future action against CBPP would require:

• Epidemiological data and information to determine and detect foci of infection;

• Effective control of animal movements from and towards these foci;

• Complete vaccine cover of cattle regularly for at least 5 consecutive years; and

• Repeat vaccination of the same cattle each year (Page 242 of the Draft Final Report: 1986-1999).

More simply, this implies close to 100% vaccination of all cattle twice a year for 5 years in addition to effective movement control.

However, since 2000 there has been limited external financial support for mass vaccination against CBPP in the countries of Central, Eastern and Western Africa. At least partially for this reason the objective of mass vaccine coverage of cattle populations of the region has, with very few reported exceptions, not been achieved. A cost recovery strategy for CBPP vaccination advocated through PACE has been implemented in most countries but this is insufficient to overcome budget deficits for implementation of effective mass vaccination. Nevertheless, as is reflected in the conclusions reached at the PACE workshop on CBPP held in Accra in February 2003, mass vaccination, whether subsidized or supplied free of charge by the veterinary services of countries, continues to be considered by most senior animal health officials in the PACE region as the preferred strategy against the disease. This is despite the fact that both the distribution and prevalence of CBPP have increased in recent years and continue to do so in the tropical regions of Africa (Report of the PACE Workshop on CBPP, Accra, February 2003). The inevitable conclusion is that existing policies are either inappropriate or are not being executed adequately.

There is a growing realisation that eradication of CBPP in the foreseeable future will be more difficult than was the case for rinderpest and probably is not a realistic possibility for the immediate future in the PACE region. If that is so, control of the impact of the disease needs to be the immediate objective (Reports of the PACE workshops on CBPP held in Addis Ababa and Accra in 2001 and 2003 respectively and report on the technical workshop of CBPP experts of 8 May 2003).

Regional options for the future

Judging from the report of the most recent PACE workshop on CBPP (Accra, February 2003) it seems that the weight of opinion among country representatives within the PACE region is that annual mass vaccination should be applied for the next 5 years - although now it is recommended that the cattle be vaccinated only once a year - to achieve control of the disease in infected regions of countries. Once that is achieved it is implied that follow-up action would be aimed at eradication of the disease although precisely what would be required in this respect has so far not been clearly articulated. The recommendations of the Accra meeting refer to a need to re-assess the effects of vaccination after 5 years. It was also recommended that areas free of infection should be protected from incursion of CBPP by vaccination (buffer) zones round the free area(s) and movement control. Ideally, buffer zones should be separated from free zones by surveillance zones in which intensive surveillance should be conducted (Report of the PACE Workshop on CBPP, Accra, February 2003).

It needs to be borne in mind that the recommendation of annual vaccination (in some cases biannual vaccination) for 5 years is based largely on empirical experience. It is only within the relatively recent past that techniques have become available for making extrapolations on the biological consequences of differing herd immunity levels resulting from vaccination. The study by Mariner (2003) is so far the only one that has utilized this approach for CBPP.

Since the Accra workshop held by PACE in February 2003, the report on the consultancy commissioned by PACE (CAPE and PEU, through FAO) and the report on the workshop of CBPP experts held in May 2003 have become available. The consultancy report based on the results of a modelling approach have provided valuable insights into the behaviour of CBPP and what will be required for its control. The study shows, firstly, that eradication of CBPP by mass vaccination alone will probably be unsuccessful. Secondly, it indicates that in order to achieve effective control (as opposed to eradication), high levels of herd immunity (³ 80%) need to be attained.

Considering these findings, the workshop of CBPP experts held in May 2003 concluded the following:

• Insufficient funding and physical resources exist within the PACE region to sustain mass vaccination as a mechanism of control; therefore, mass vaccination would only be sustainable if significant outside funding support becomes available;

• Poor quality vaccines that induce ephemeral and/or poor immune responses are a problem for effective CBPP control in the PACE region;

• T1-44 vaccine, because it is inclined to produce post-vaccinal reactions that are unacceptable to livestock owners, constitutes a disincentive to widespread vaccine use for sustained periods of time (at the least it would require funds to compensate owners for losses resulting from post-vaccinal reactions);

• Lack of an in vitro test to differentiate vaccinated from unvaccinated cattle complicates control where vaccines are employed;

• Lack of trust and co-operation between some veterinary services and the livestockowning communities they serve is a significant problem.

This situation leaves AU-IBAR with two alternatives:

1. Devise a regional mass vaccination programme to which donor organizations could be persuaded to contribute that would make up the financial shortfall in funding from country contributions and cost recovery on the one hand and the full cost of mass vaccination on the other; or

2. Develop an alternative strategy.

These two alternatives are discussed in more detail below.

Regional mass vaccination programme

The cost of such a programme, covering a 5-year period (whether the cattle were vaccinated once or twice a year) is likely to be high (see Table 1). The data in Table 1 were derived from information based on the costs of vaccination against CBPP during PARC in 10 countries. It shows the calculated cost of vaccinating 70% of the cattle in the selected countries annually over a 5 year period. This level of vaccine cover was selected because it is: (1) unlikely that all cattle in any country could be consistently vaccinated, and (2) most countries have zones within the country where vaccination is not traditionally practiced because CBPP has little or no impact in those zones (some are claimed to be free of the infection). It is evident that if a high level of vaccination coverage were to be achieved in the >30 countries that constitute Central, Eastern and Western Africa, the overall costs would be approximately three times greater than those shown in Table 1, i.e. > € 300 million. It is possible that up to half of this cost could be recovered from the cattle owners but even so a sum of € 150 million is large and probably unrealistic in comparison with previous aid projects directed towards animal health.

Table 1. Total cost (€) of CBPP vaccinations in ten countries (70% mass vaccination scenario)

Assumptions:

1. Cattle population increasing at 1% per year over the base scenario.
2. 70% vaccination coverage.
3. Depreciation of capital equipment from 20% year 1 down to 65% by year 5.

Furthermore, it is unlikely that such a large sum of money would be made available by donors for an animal disease unless there was good reason to believe that it would result in the eradication of the disease and that the extent of the return on the investment could be shown to be at least several-fold higher than the sum invested in the programme. It should also be noted when considering donor support that most European donors link their funding to millennium goals of poverty alleviation and freedom from hunger and the PRSPs whilst USAID is linking its funding to good governance and business development. Merely showing a benefit to cost is unlikely to be sufficient incentive for donor support in the near future.

As already stated, the modelling study of Mariner (2003) indicates that eradication through vaccination alone would be unlikely to succeed. Even effective control over a wide area would require herd immunity levels of around 80% that were hardly ever achieved against rinderpest during PARC. Taking all this into consideration leaves little room for optimism that a mass-vaccination programme against CBPP on its own would be either affordable or effective. Based on experience elsewhere in the world and that from Africa in previous decades, an effective programme would require, in addition to high vaccination coverage, good control over the movement of infected or potentially infected cattle into areas where vaccine is being applied. This would necessitate additional costs, some indirect and essentially hidden resulting from limitations imposed on the choices of livestock keepers, pastoralists especially, in respect of free movement of their animals. Mass vaccination for 5 years therefore has limited prospects for success in the long term.

Alternative strategy

Because CBPP is endemic to many regions of Africa between the Sahara and 15° S, livestock owners have to live on a daily basis with the consequences of the disease, i.e. its erosive effects and periodic epizootics.

It was generally conceded at the two PACE workshops on CBPP held in Addis Ababa and Accra that antibiotic treatment of cases of CBPP is a widespread practice throughout the PACE region. This is despite the fact that treatment of CBPP cases is actively discouraged in many PACE countries and even illegal in some. Antibiotics usually have to be bought by the owners and therefore treatment of cattle for CBPP and other diseases costs owners hard currency which they can ill afford. Conversely, when it comes to administration of vaccine few owners, certainly those in rural areas, have access to vaccine through drug dealers, community-based animal health workers (CAHWs) or private veterinarians. This creates a dichotomy in the approach to CBPP in most countries: the official veterinary service applies vaccine (usually with cost recovery) in areas and at frequencies that they dictate while treatment is discouraged or illegal and at the exclusive cost of the owner. This means that some owners who would like to have their cattle vaccinated have no means of having this done.

The efficacy of treatment for CBPP, as agreed at all the recent workshops held by PACE on CBPP, is largely unknown as are the epidemiological consequences of treatment (possible creation of carriers) despite the fact that livestock owners obviously consider it beneficial. Studies into this issue are ongoing and some are being funded at least partially by PACE. The results are clearly important and anxiously awaited. However, pending the outcome of these studies it is intuitively probable that the best approach to the control of CBPP would be to regularly (say every 6 months) vaccinate cattle in endemically infected areas or those at risk of being infected while treating and, if possible, isolating individual animals when they develop clinical disease. In this way the benefits of both vaccination (creation of high levels of herd immunity) and treatment (enabling animals that would otherwise die or be seriously debilitated to recover) would hopefully act synergistically to reduce losses. The scientific evidence required to recommend the use of a particular antibiotic against a particular microbial agent is based on in vitro antibiotic sensitivity tests and determination of minimal inhibitory concentrations reached in various tissues and secretions as well as, where possible, controlled trials. In the case of CBPP, published information on the sensitivity of M. mycoides subspecies mycoides (small colony) to oxytetracycline (and tylosin) is available and demonstrates sensitivity to these drugs. As there is no scientific evidence to support the hypothesis that the use of these drugs causes a chronic infective CBPP state, there is no scientific reason currently not to use them to treat CBPP.

Mariner (2003) has suggested that elective vaccination of cattle (i.e. the owner decides whether to vaccinate or not and is responsible for the payment for such vaccination) in pastoral areas may be more effective and sustainable than mass vaccination conducted by official veterinary services. He has pointed out that for this to happen would require liberalising the distribution and availability of vaccines against CBPP. Furthermore, Mariner’s study has shown that even if elective vaccination was patchily adopted, the benefits to the herd-owners who vaccinate their cattle would not be negated by neighbours who fail to do so.

Bearing the above in mind, a somewhat different approach to CBPP control can be considered. The alternative approach is based on enabling owners, either through private practitioners (or possibly veterinary-supervised paraprofessionals such as CAHWs) operating individually or on behalf of co-operatives, to vaccinate and, where necessary, treat their cattle to control CBPP. This presupposes that official veterinary services would support this process by:

• Enacting enabling legislation to permit non-official vaccination and treatment;

• Supply of vaccine and drugs in locations, under conditions (refrigeration) and quantities (small dose packs) that owners would find helpful.

Ideally, some form of management of the movement of cattle from areas where CBPP is a problem disease to areas that are free or relatively free of the disease, would favour better control than vaccination and treatment alone. Circumstances will dictate where that is possible and where not. However, it needs to be ensured that such movement management measures do not cause greater losses to the livestock industry than the disease itself. Veterinary authorities in Africa have consistently underestimated the knock-on effects of animal health control measures, which is one of the reasons why disease control measures that livestock owners find onerous are often ignored or surreptitiously avoided.

This proposal therefore envisages official veterinary services providing support to livestock owners to control the disease privately rather than physically directing and implementing vaccination and discouraging treatment. This would likely greatly reduce the cost of control to the public sector and enable more effective control for those that want, and are willing, to pay for it.

Clearly, this policy option is contrary to that adopted officially by many countries in the PACE region as well as that recommended internationally. It may also not appeal to many official veterinary services because actions directed towards control/eradication of CBPP are a major focus of their activity. On the other hand, it would overcome the problem of unaffordable - and therefore poorly implemented - vaccination programmes with unrealistic expectations that continually fail to meet their objectives. This unfavourable situation is unlikely to change in the foreseeable future unless, as indicated above, massive additional investment in CBPP control occurs.

CBPP vaccine quality is critical to its efficacy in the field and acceptability to farmers who are expected to pay for the cost of CBPP vaccination. Revival of vaccine quality assurance capacity at regional or pan-African levels is important to ensure good quality products. It is obviously untenable to expect livestock owners to pay for a product that does not reach minimum standards. Ultimately, it is the governments’ responsibility to ensure that vaccines and antibiotics available to the public sector are of a suitable standard.

The devolution of CBPP control to the livestock owner would also create difficulties in accepting that a whole region of Africa would tacitly acknowledge that it is unable to eradicate a List A disease that has been eliminated from much of the rest of the world. This is likely to create difficulties in trading live animals but there are other ways of addressing this problem. For example, establishing disease-free or export zones of limited size that could either be kept free of CBPP or where measures could be instituted to reduce the risk of spread of the infection through trade are possible. Such approaches would enable international trade from a country that is otherwise not free of CBPP and would also create nuclei of infection-free cattle that could form the basis of a future eradication strategy.

If this approach were to be endorsed by IBAR and the PACE countries, it may be possible to turn CBPP control into a more palatable option (than mass vaccination) for donor support. Liberalising the use of the vaccine could be viewed as a way of stimulating the private sector delivery of veterinary services. The formation of export zones or systems that create wealth and have a trickle down effect to the poor is similarly likely to be more appealing to some donors than subsidizing mass vaccination campaigns. USAID, for example, is already heavily investing in promotion of livestock trade. The European Commission is increasingly interested in both trade and poverty alleviation.

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