Vital Elements for the Successful Control of Foot-And-mouth Disease by Vaccination

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Vital elements for the successful control of foot-and-mouth

disease by vaccination

A.J.M. Garland *

`Collingwood', Dawney Hill, Pirbright, Surrey GU24 0JB, UK

Abstract

The ecient control of foot-and-mouth disease (FMD) by immunisation depends not only on the appropriate choice of

vaccine in terms of innocuity, potency and strain composition, but also on a series of inter-related zoo-sanitary factors which are

equally important. These include: national, centralised planning (including contingency planning) and control; vaccination andrevaccination policy; the availability of epizootiological intelligence based on adequate diagnostic capability and ongoing

immunological surveillance; the logistics of supply with its components of storage, transport and distribution; proper vaccine

application; cleaning and disinfection of premises, vehicles and personnel; identi®cation of individual animals; control of animal

movement; recording; ongoing economic outcome and bene®t analyses; training and retraining of professional and technical

sta; public relations and especially the commitment of the agricultural community. These elements are reviewed in this paper.

# 1999 Elsevier Science Ltd. All rights reserved.

1. Introduction

In the 70 years which have elapsed since the ®rst

publications appeared on vaccination against foot-and-

mouth disease (FMD) [1], major advances have been

made in virtually all aspects of our understanding of

the virus, the disease and the methods for its control.

Studies in areas including: the molecular biology of the

virus; the pathogenesis of the disease; the excretion,

dissemination and persistence of the virus; the epide-

miology of the disease; the immune response; the gen-

etic and antigenic relationships between strains of virus

and the reliable production of safe and potent

vaccines [2] have all provided information which has

been applied in increasingly eective approaches to thecontrol of FMD. Nevertheless, and despite spectacular

success in many countries where the disease was for-

merly endemic, large areas of the globe continue to

suer the depredations of FMD. The reasons for these

failures are complex, but insucient attention to basic

elements of planning and resource in the prosecution

of control schemes can be critically important.

2. Centralised planning and control

While control schemes for FMD may be aimed in-

itially at the local reduction of infection, of disease

severity and of disease incidence and prevalence, the

ultimate aim should be the total eradication of the dis-

ease. In endemic areas the approach taken will vary

according to local circumstances. However, the ulti-

mate goal is inevitably attained in stages. Thus the dis-

ease and measures for its control progress from

endemicity at the initiation of mass vaccination, mov-

ing through increasing control of sporadic outbreaks,

to the status of `freedom from disease with vacci-

nation' and ®nally to the status of `freedom from dis-

ease without vaccination', a progression known as `the

OIE pathway' [3]. Each of these stages has associated

criteria, as described in the International Animal

Health Code of the Oce des Epizooties (OIE) [4],

and each has international trading implications for live

animals and animal products.

It is important to recognise that vaccination is only

one of several zoo-sanitary measures which are essen-

tial for the control of FMD and that vaccination alone

cannot be relied upon for a successful outcome. The

Vaccine 17 (1999) 1760±1766

0264-410X/99/$19.00 # 1999 Elsevier Science Ltd. All rights reserved.

P I I : S 0 2 6 4 -4 1 0 X (9 8 )0 0 4 4 3 -5

* Tel.: +44-1483-473-476; fax: +44-1483-480-023.



disease has extreme communicability and the modal-

ities for its dissemination are very numerous. Some

modes, such as airborne spread, are virtually imposs-

ible to prevent. Moreover, the duration of immunity

following inactivated FMD vaccination is short rela-

tive to that of many other vaccines (particularly live

vaccines) and it is unlikely that immunity can be con-

tinuously maintained at a protective level in all indi-

viduals within the national herd and/or ¯ock. Forthese and other reasons the strategy should include

mass revaccination biannually or even triannually,

depending on the characteristics of the vaccine

employed, and possibly special reinforcement of vacci-

nation in strategic areas (e.g. barrier vaccination in

vulnerable border areas) and ring vaccination around

foci of disease. Additional zoo-sanitary measures are

also essential. These include:

. Control of legal and illegal animal movement within

the country.

.Prohibition of the import of susceptible animals andcertain animal products from areas with a high risk

of FMD infection.

. Application of risk assessment and risk management

for the importation of susceptible animals and ani-

mal products from areas with an acceptable risk of

FMD infection.

. Appropriate pre-testing of susceptible animals for

FMD prior to import and the application of quar-

antine measures.

. Control of foci by restricting the movement of ani-

mals and animal products from the infected area

and by the disinfection/safe destruction of infected

and potentially infected materials.

. Application of a slaughter policy for infected and

susceptible, in-contact animals, as justi®ed by the

overall epizootiological situation.

Eective mass vaccination depends to a great extent

on co-ordinated, centralised planning, organisation

and control. This responsibility is usually vested in the

National Veterinary Service. The department con-

cerned must be adequately staed in terms of numbers

of experienced, knowledgeable personnel and be pro-

vided with the necessary physical and ®nancial

resources.The areas of expertise which, ideally, should be

available to the central authority include:

. Epidemiology (with specialised knowledge of FMD).

. Animal health legislation.

. Veterinary/agricultural economics (including cost/

bene®t analysis).

. Risk analysis (assessment and management).

. Logistics.

. Information technology.

. Training and education.

In an ideal situation the headquarters team should

have access to the following data and resources:

. Species, numbers and locations of susceptible live-

stock (cattle, bualo, sheep, goats, pigs).

. Systems of animal management and marketing

employed.. Routes of animal movement both legal and illegal

(cross border trade movements, movement for

breeding, fattening, slaughter, transhumance, etc.).

. Location of particularly valuable livestock (arti®cial

insemination stations, pedigree herds/¯ocks, etc.).

. Availability/non-availability of aids to animal man-

agement for vaccination (cattle races, crushes, etc.).

. Availability of climatic data (rainy seasons, drought

periods, etc.).

. Disposition and condition of vaccination equipment.

. Location and condition of cold stores, cool boxes,

gel packs and temperature monitors.. Availability and condition of protective clothing

(overalls, rubber boots, possibly waterproof clothing

and gloves).

. Availability of disinfectants and disinfection equip-

ment (nail and boot brushes, pressurised spraying

equipment).

. Availability and condition of transport.

. Availability and competence of manpower (veteri-

narians, animal assistants, vaccinators, administra-

tive sta).

. Availability of a system of identi®cation and regis-

tration of individual animals.

. Availability of recording systems (manual and/orcomputerised).

. Availability of suitable vaccine (correct antigenic

composition, correct formulation, safety data and

potency data in compliance with international stan-

dards, adequate remaining shelf-life).

. Availability of written Standing Operating Pro-

cedures (SOPs) for all aspects of vaccination (vacci-

nation, revaccination, ring vaccination, etc.).

. Availability of written contingency plans.

. Existence of appropriate national legislation de®ning

the responsibilities and powers of the Ministry of

Agriculture/Veterinary Department for all aspects of the control of FMD, including, for example, legis-

lation on the enforcement of compulsory vacci-

nation; the collection of fees as appropriate; and any

penalties for non-compliance.

. Access to current research information relevant to

the control of FMD.

This checklist summarises the principal data and

equipment to be assembled and/or considered in plan-

ning for mass vaccination. The manuals for the control

A.J.M. Garland / Vaccine 17 (1999) 1760±1766 1761



of rinderpest published by the Food and Agriculture

Organisation also provide useful guidance [5] although

the vaccine in this case is a live attenuated preparation.

Additional useful information is available in textbook

form [6±8] and in international legislation such as

European Union Directives and Guidelines.

A further important option to be considered is that

of the possibility of combining elements of disease con-

trol schemes, for example, by vaccinating againstFMD, rinderpest and sheep and goat pox simul-

taneously.

Some items listed above are desirable rather than

essential. Local conditions make some aspects more

important than others and successful campaigns have

been mounted in the absence of some of these el-

ements. A notable example might be the absence of a

national system for the identi®cation and registration

of individual animals. Some elements are concerned

with measures other than vaccination per se (e.g. disin-

fection between farms and/or in the event of discover-

ing clinical FMD) and many have application beyondthe speci®c control of FMD in the general ®elds of hy-

giene, animal health, animal production and disease

control.

The importance of written plans, contingency plans

and SOPs is emphasised, as is the need for a calendar

for the routine critical review of these documents at

least annually [6±9]. These provide a formal structure

for the campaign, aid consistency of approach and are

very valuable aids in training and education. A further

requirement is that of carrying out simulation exercises

annually or more frequently as necessary. These are

used in training and also to test out the practical

aspects of theoretical methodology and procedures.Documentation should be revised appropriately in the

light of the results of such simulations.

Other desirable functions of the headquarters sta

are in the performance of cost bene®t and risk bene®t

analyses, providing the basis for decisions on the

adoption of various options and strategies for the

control of FMD, and other diseases, and in monitor-

ing the progress of the programmes during

implementation [10±13].

Having de®ned the overall campaign strategy the

detailed plans for implementation are drawn up. The

plans should include timetables for the assembly of materials and equipment and for successive rounds of

vaccination and revaccination at speci®c locations.

Allowance must be made for the immunisation of suc-

cessive generations of new-born animals and for inter-

ference in their vaccinal response due to maternal

immunity. The time taken to achieve coverage is also

an important aspect, since the more rapidly an area

can be vaccinated, the sooner will levels of herd immu-

nity be established capable of minimising the amount

of virus circulating in the environment.

3. Epizootiological intelligence and diagnosis

Comprehensive and up-to-date epizootiological in-

formation is a prerequisite for eective disease control.

Within a country or region, information on the status

of a particular disease can be gathered by veterinar-

ians, in both the private and public sectors, and even

earlier and more eectively by an educated livestock

community. In the case of FMD the noti®cation pro-cedure is usually reinforced by the designation of the

disease in national legislation as being compulsorily

noti®able on the basis of suspicion of the presence of

disease on clinical grounds. The national veterinary

service usually has the responsibility for the con®r-

mation of the presence or absence of FMD by means

of expert clinical examination, epidemiological investi-

gations and laboratory testing of suspect samples.

Such samples are preferably of fresh vesicular lesion

material or, in the case of asymptomatic fatalities, of

cardiac muscle. However samples may also be of

serum, milk or oesophageal±pharyngeal ¯uid.The overall speed of obtaining samples of lesion ma-

terial can be accelerated by the preparation of sample

bottles containing glycerol-phosphate buer at pH 7.0

and their advance distribution to veterinary establish-

ments at strategic locations.

Samples for antigen or antibody detection and/or

assay may be tested by several dierent techniques at

various levels of sensitivity. The long established

method of complement ®xation (CF) continues to ®nd

application for the typing of FMD virus in a few lab-

oratories, although enzyme linked immunosorbent

assays (ELISAs) of various descriptions have been

increasingly used for both antigen and antibody identi-®cation and assay [14, 15]. ELISA oers signi®cant ad-

vantages of sensitivity, speci®city and objectivity over

CF tests and is the preferred, optimal method as pre-

scribed by OIE [4]. Passage of ®eld samples in suscep-

tible animals or, more commonly, susceptible tissue

cultures may also be used to amplify small amounts of

infectious virus.

Of the other advanced techniques, as yet restricted

to a limited number of laboratories, the polymerase

chain reaction (PCR) method has the advantage of

being able to detect minute amounts of viral RNA,

even in the absence of infectious virus. Nucleic acidsequencing of selected portions of the RNA genome

allows for the precise characterisation of virus isolates

and their comparison with the sequences of reference

strains held in data banks. These molecular techniques

have particular application in de®ning the relationship

between a current ®eld isolate and existing ®eld and

vaccine strains of virus and can assist in the identi®-

cation of the origin of outbreaks [16].

While the characterisation of virus isolates may well

be eected in national laboratories and regional FMD

A.J.M. Garland / Vaccine 17 (1999) 1760±17661762



laboratories, it is also strongly advisable to submit

representative samples to the OIE/FAO World

Reference Laboratory in order to con®rm the diagno-

sis and to enable the detailed classi®cation of the

sample in relation to other existing strains. Samples

must be despatched in accordance with established

procedures for the preservation of viral infectivity

and the maintenance of disease security in transit,

including compliance with current international postalregulations [17].

National epizootiological intelligence should be sup-

plemented by the continual exchange of information

between neighbouring countries within a region and,

most importantly, by the prompt exchange of infor-

mation with the international authorities including: the

OIE in Paris, France; the Food and Agriculture

Organisation (FAO) of the United Nations in Rome,

Italy and the OIE/FAO World Reference Laboratory

at Pirbright in the United Kingdom.

4. Diagnostic laboratory capability

Many countries maintain virological laboratories

equipped for the diagnosis of FMD and the serological

surveillance for both the disease and the immune sta-

tus of herds and ¯ocks in which vaccination has been

applied.

Much of this work can today be eected without the

necessity to employ live virus by the use of inactivated

viruses and non-infectious viral components. This

approach is to be commended. However, it is to be

noted that where the work involves material which isknown, or suspected, to contain infectious virus,

such laboratories should be operated under full

disease security in compliance with international

recommendations [4]. Desirable procedures in this con-

text are adherence to the disease security recommen-

dations formulated by the European Union, Standing

Veterinary Committee's Expert Group in FMD disease

security and the inspection and approval of the labora-

tory by this group [18].

Laboratory sta should maintain an awareness that

FMD exists as seven immunologically distinct but

clinically indistinguishable virus types and that newstrains of FMD can and do emerge from time to time.

Such antigenic drift was exempli®ed by the A22 strain

which ®rst appeared in Iran in 1964 and which sub-

sequently spread to be the most common subtype

throughout the Near Eastern countries. More recently

this phenomenon has again been demonstrated by the

emergence and dissemination of a new type A strain,

antigenically and genomically distinct from all other

known strains of type A virus, which is now prevalent

in Turkey.

FMD virus types historically absent from a region

may occasionally migrate, as seen with South Africa

Type 1 (SAT 1) which moved rapidly through the

Middle East and as far north as Turkey and Greece in

1962. Similarly Type Asia 1 penetrated into Turkey in

1973. Yet again, existing diseases or completely novel

diseases which resemble FMD clinically may appear

and/or reappear, such as vesicular stomatitis, vesicular

exanthema of pigs and swine vesicular disease, the lat-ter appearing in Italy and elsewhere from 1966

onwards. Laboratories should therefore have the capa-

bility for dierential diagnosis. The practice of some

laboratories to test suspect samples of FMD virus only

for types and strains of FMD which are known to be

prevalent in that region must be recognised as carrying

at least a potential risk.

Apart from diagnosis such laboratories can under-

take serological surveillance. Studies of this type

should have clearly de®ned objectives, such as the in-

vestigation of antibody levels in the national herds and

¯ocks after vaccination and revaccination or of thepresence of sub-clinical FMD, as may be encountered

particularly in sheep and goats. The surveys should

have a sound statistical basis and should include an el-

ement of sequential sampling of speci®ed herds, ¯ocks

and individuals. In future FMD laboratories are also

likely to have the valuable capability to dierentiate

between antibodies induced by vaccination and infec-

tion, using assays for non-structural proteins of FMD

virus [19].

A further recommendation is that FMD laboratories

should be accredited in terms of human and physical

resources and technical capability in compliance

with international norms (e.g. OIE Guidelines forLaboratory Quality Evaluation [20] and OIE

Guidelines for Laboratory Pro®ciency testing) [21].

Moreover the tests employed should be calibrated and

performed in compliance with international standards

wherever possible [4]. Participation in the ongoing

exercises for the standardisation of tests as organised

under the auspices of OIE/FAO is valuable in this

context [22].

5. Selection of FMD vaccine

There are currently a number of commercially man-

ufactured vaccines available of diering strain compo-

sition, antigenic content, adjuvant formulation and

cost [2]. All are produced using inactivated antigens.

Vaccine is available as fully formulated and tested pro-

duct or, more usually in emergency situations, it can

be freshly formulated from concentrated, inactivated

antigen(s) stored at low temperature in vaccine banks

maintained by commercial manufacturers or by

national and international authorities [23].




In selecting the appropriate vaccine or vaccines a

number of factors must be taken into account.

The ®rst is that the antigenic composition of the

vaccine, mono- or polyvalent, should give immunity

against the virus strain(s) known to be prevalent in the

region or those considered most likely to be intro-

duced.

The second is that the vaccine should have been sat-

isfactorily tested for innocuity and potency accordingto international standards as detailed in national or in-

ternational pharmacopoeias, e.g. as in the European

Pharmacopoeia [24] and/or the recommendations of

the OIE [4]. In terms of potency the present pharmaco-

poeial requirement is that the vaccine should have

been shown to contain at least three 50% protective

doses (PD50) per vaccine dose volume. However,

many of today's commercially available vaccines con-

tain greatly in excess of 3 PD50 per dose and the

Research Group of the European Commission for the

Control of FMD has recently recommended that vac-

cines should contain a minimum of 6 PD50 per dosefor routine prophylaxis and 10 PD50 per dose for

emergency use. There is evidence that the higher the

antigenic content of a vaccine, and thus usually the

potency, then the wider the spectrum of antigenic

cover that will be engendered and the longer the dur-

ation of immunity which will persist [23]. Experimental

vaccines have been reported formulated with very high

levels of antigen giving PD50 values in the order of

100 PD50 per dose and protection lasting for at least

one year [25]. However, the cost of vaccine is also re-

lated to the level of incorporation of antigen and a

balance has to be struck between vaccine potency, vac-

cine cost and available funds.The third factor is that of the vaccine adjuvant. The

most common adjuvants are aluminium hydroxide

plus saponin in aqueous (AS) vaccines and oils and

emulsi®ers in various oil emulsion (OE) vaccines.

Broadly speaking, and depending on the individual

vaccine, OE vaccines are claimed to engender longer

lasting immunity than AS vaccines following primary

vaccination and so require less frequent boosting. AS

vaccines are suitable for the immunisation of rumi-

nants but give very poor responses in pigs, whereas

OE vaccines provide immunity in both ruminants and

pigs. Maternal immunity can interfere with the ecacyof the response to AS vaccines, whereas OE vaccines

are signi®cantly less eected in this way. OE vaccines

are more costly than AS vaccines and concerns have

been expressed over the association of OE vaccines

with persistent carcass reactions. Once again a balance

must be struck between the various characteristics of

the available vaccines in selecting the most appropriate

formulation.

The fourth factor is that of the stability of the vac-

cine and the question of its expiry date. Most FMD

vaccines claim a shelf life of 12 to 24 months post-test-

ing. Ideally the vaccine should be obtained from the

manufacturer with the longest possible remaining shelf

life, or at least with sucient remaining shelf life to

allow adequate time for the use of the vaccine in the

®eld prior to its expiry.

The ®fth factor is the availability of the chosen vac-

cine formulation in sucient quantity to enable the

completion of the planned vaccination campaign(s).Calculations of the number of doses of vaccine

required should take into account both vaccination

and revaccination and allow for a certain amount of

wastage, for example when part used vaccine bottles

are discarded according to good practice at the end of

a day's work and/or between farms. Allowance must

also be made for possible supplementary, ring vacci-

nation in emergency situations.

6. The cold chain

FMD vaccines must be maintained under refriger-

ation for the optimal retention of antigenic potency,

usually at 4228C. The antigen loses immunogenic ac-

tivity progressively as the storage temperature

increases above these levels [26]. In addition freezing

and thawing of FMD vaccines damages their integrity

and can also cause the breakage of both aluminium

hydroxide gels and oil emulsions, decreasing and poss-

ibly destroying the immunogenicity of the vaccines.

The eciency of the cold chain is therefore a critical

factor for optimal vaccine storage.

The cold chain includes all the refrigerated storage

of the vaccine from the time of manufacture, throughvehicular and air transport, warehousing and distri-

bution, to the point of inoculation into the animal.

Shipments of vaccine should be in thermally insulated

containers, possibly with gel packs and accompanied

with validated temperature monitoring and/or record-

ing equipment. Domestic refrigerators and walk-in

cold rooms should be ®tted with temperature recorders

which are calibrated against international standards

and regularly revalidated. Cool boxes used to trans-

port vaccine should be tested to determine the time for

which they are capable of maintaining vaccine at the

recommended storage temperature under conditionswhich simulate the most extreme environmental tem-

peratures likely to be encountered in the ®eld. Portable

refrigeration equipment should be subjected to regular

maintenance and routinely tested prior to use.

7. Training and education

Veterinarians, animal technicians and vaccinators

should be educated, trained and tested to appropriate




levels in good vaccination practice, good hygienic prac-

tice, disease control and legislation. Plans, contingency

plans and SOPs are valuable aids in this area. Topics

to be covered may include:

. The disease and its eects.

. The care of vaccine and vaccination equipment,

including the sterilisation of syringes and needles.

. Vaccine application (site(s) of inoculation, dose ratesfor dierent species).

. Cleaning and disinfection of persons, protective

clothing, equipment and vehicles.

. Recording.

. Animal handling.

. Animal identi®cation.

. Taking and treatment of samples.

. Means of managing any outbreaks of FMD (or

other diseases) which they may encounter.

A most important aspect is the appreciation by such

sta of the role which they can inadvertently play in

the spread of FMD and other communicable diseases

between farms. Supplementary training may include

such topics as the collection and recording of fees and

®rst aid. Training records should be kept and refresher

courses organised.

8. Logistics of supply and distribution

Ideally vaccine will be ordered with the maximum

remaining shelf life and in quantities appropriate to agiven phase of the vaccination campaign. The aim

should be to attain at least 80% and preferably 100%

vaccine coverage of susceptible livestock. Lesser levels

of coverage and the use of vaccines of poor potency

are likely to be associated with inecient control and,

importantly, with the selection of antigenic mutants in

partially immune animal populations. It is to be recog-

nised, however, that decisions have sometimes been

made to vaccinate only certain species, such as cattle,

bualo and pigs and to ignore small ruminants,

usually on the grounds of cost. This approach may

well carry the risk of perpetuating the disease.Vaccine should be removed from the central cold

stores only in sucient quantity for the day's work

and the movement and utilisation of vaccine will be

recorded in respect of the date, the number of bottles

and doses removed, the location at which they were

used, the numbers of doses utilised according to

species and the number of doses discarded. Standard

record forms should be used which also allow for sup-

plementary notes (e.g. on the number of young stock

which may need to be re-vaccinated and when).

Vaccine discarded at the expiry of its validity, or for

any other reason, should be safely destroyed, securely

disposed of and its fate recorded.

9. Public relations

The commitment of the farming community to

schemes of animal disease control can greatly facilitatesuccess. Conversely, the lack of their commitment ren-

ders the task much more dicult. This is particularly

evident when there is an element of cost to the farmer.

For these reasons it is important to use all available

means to publicise control measures for FMD and to

explain the rationale, the legal requirements, the time-

table and the bene®ts which are expected to accrue

from their implementation. Media which can be uti-

lised for these purposes include: lea¯ets, newspapers,

magazines, trade journals, radio and television.

Meetings can also be arranged with associations, or-

ganisations and clubs connected with agriculture, andparticularly with livestock, such as Farmers Unions,

Collectives, Co-operatives, Breed Associations, etc.

Use can also be made of veterinary schools, agricul-

tural colleges and extension services for these purposes.

The public awareness campaign should be planned in

advance and should also allow for the messages to be

reinforced periodically, ideally with bulletins describing

the ongoing success of the control scheme.

10. Conclusions

Despite the complexity of FMD in terms of the mul-tiplicity of types and strains, the wide host range and

the highly contagious nature of the disease, vacci-

nation campaigns combined with other zoo-sanitary

control measures have been attended with notable suc-

cess in many parts of the world. A conspicuous

example is found in continental Europe where mass

compulsory vaccination together with the control of

the movement of live animals and of animal products,

sometimes combined with the slaughter and destruc-

tion of infected animals, reduced the incidence of the

disease from being endemic throughout much of the

twentieth century to the point at which vaccinationwas could be totally discontinued in 1990/1991.

Similarly, in South America, decades of endemic FMD

are now coming under control following renewed vac-

cination campaigns in many countries utilising OE vac-

cines. Thus Chile and Uruguay have attained the

status of freedom without vaccination, while Paraguay,

Argentina and the southern states of Brazil have

reported no outbreaks for several years and have

applied to OIE for recognition of the status of freedom

with vaccination. These examples demonstrate what




can be achieved when all the elements of control are

successfully combined, including the use of vaccination

campaigns which have been carefully planned, ade-

quately resourced and eectively administered.

Acknowledgement

I thank Dr. A.I. Donaldson for his critical review of the manuscript.

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