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THE RINDERPEST DEADLINE - Sir Gordon R. Scott

Courtesy : Festschrift - Dr. S. Ramachandran

Morbilliviruses are a clade of animal and human plagues descended aeons ago from rinderpest virus. The related terrestrial viruses are peste des petits ruminants, measles, canine distemper, and its aquatic viruses are phocine and cetacean distempers. Their epidemiological behaviour is very characteristic; if they infect a naïve host population they provoke epidemics and pandemics that kill thousands. If the host population is large, epidemics may become persistent endemics restricted to the young with waning maternal immunity. All the clade are excellent immunogens producing life-long immunities in fully susceptible hosts.

Rinderpest, for centuries, was the most dreaded bovine plague known and its causative virus belongs to a select group of notorious pathogens that have changed the course of history more than once. Its ravages are fuelled by the frequency of wars in Asia and Europe. The principal vehicle of dissemination, favoured by military commanders, were large Grey Steppe oxen ideally suited to the roles of draught and pack animals. Their long association with rinderpest virus has produced a high innate resistance manifested by slow spread of the infection among them and, when infected, by the absence of overt clinical signs. A troop of Grey Steppe cattle could shed rinderpest virus over months ensuring more virgin- soil epidemics in looted beasts. Work oxen of the conquered nations died in their thousands, fields were left untilled, farming collapsed, starving peasants migrated into the cities overwhelming the machinery of government.

Commercial dissemination of rinderpest was limited to cattle moving on foot between fairs and markets and to a few short-sea shipments. A new dimension was added in the middle years of the 19th century with the development and exploitation of steam-power. Cattle were railed and shipped in numbers previously impossible. The sequel was inevitable; the Russian Empire suffered rinderpest pandemics in Asia and Europe. In 1887, the Italian army was regrouping to attack Abyssinia. They purchased a shipload of infected cattle in India that were disembarked at the Red Sea port of Massawa. The disease swept from the Horn of Africa westward to reach the Atlantic coast of Senegal in 1892, and southward to Cape Colony in 1897. Africa south of the Sahara had never before been exposed to rinderpest virus and the inevitable pandemic killed off most of the cattle and wildlife of the continent.

The nature of rinderpest was unknown until Dr. Bernardo Ramazzini, Professor of Practical Medicine at the University of Padua studied a fresh invasion of the disease in imported trade cattle in 1709 with such thoroughness that he is rightly recognised as the Father of Veterinary Epidemiology (1). He confirmed the contagious nature of rinderpest stressing that its mode of spread was limited to close contact between sick and healthy animals. He described the evolution of the clinical signs from the onset of fever to death seven days later and correlated them with the post-mortem findings. The analysis of his data established the source and route of the epidemic. 

Prior to the 18th century, prayers and so-called cures failed to limit the havoc of rinderpest outbreaks. In 1713 a solution was found; His Holiness Pope Clement XI instructed his personal physician, Dr. Giovanni Lancisi, to investigate a murderous plague then raging among the church’s herds and to prescribe measures for its suppression. Dr. Lancisi identified the plague as rinderpest and formulated recommendations for its containment by banning the use of cures and by killing the sick and in-contacts immediately (2). The penalties for transgressors were drastic; guilty laymen were to be hung, drawn and quartered whereas guilty ecclesiastics were to be sent to the galleys for life. His edicts were broadcast from church pulpits with the result that the disease was arrested within nine months whereas the rest of mainland Europe suffered a continuity of outbreaks fanned by wars for nearly 100 years.

In mid-century the catastrophic pandemic devastated all countries in Europe by killing 200 million cattle that created an awareness for the need for trained manpower and national infrastructures to handle animal diseases. The first veterinary school was founded in France in Lyon and within a year the Principal and his pupils were in the field tackling rinderpest. Most European countries followed and, in addition, enacted legislation to control animal movements to limit the spread of disease. 

The idea of “pestisation” of healthy cattle stemmed from Ramazzini’s belief that rinderpest mimicked human smallpox. He tested the hypothesis in 1711 by injecting cattle with setons soaked in morbid discharges collected from a sick animal; the results were not encouraging. Nevertheless, investigators in most European countries inoculated cattle with infected discharges. Dr. A. Koch calculated that in the 18th century 13,000 cattle were subjected to pestisation, the average mortality being 25 percent (3). The technique was abandoned in 1874. 

The 18th century’s western pandemics petered out early in the 19th century. Endemic rinderpest, however, still existed in Asia and was the source of fresh epidemics in Europe and Africa. The disastrous English outbreak in 1865 was due to the first commercial steamer shipment from Russia disembarking infected cattle at Hull. Within 24 hours the animals were up for sale in London’s Metropolitan market. The resultant epidemic was belatedly contained by the application of Lancisi’s recommendations in 1867. The disease spread to mainland Europe infecting the western states. European countries closed their Russian borders to cattle stimulating the Tsar to found several Rinderpest Experiment Stations in 1860 to elucidate the cause of rinderpest and to develop methods of its control. The Dorpat group led by Professor E. Semmer found in 1893 that if serum collected from recovered cattle was inoculated into susceptible cattle they were protected against rinderpest (4). Shortly thereafter the Great African Rinderpest Pandemic hit South Africa and the prophylactic role of antiserum was confirmed. Anti-serum alone was in vogue until the 1920s but its protection was short-lived. Aid personnel from Europe developed the antiserum - virus simultaneous method of immunisation which conferred a life-long resistance. 

The continental pandemic burnt itself out in southern Africa early in the 20th century. Unfortunately, the infection persisted endemically in most African states north of 10 degrees south. Rinderpest was endemic also in several countries in Asia including China and were the sources of epidemics in Indonesia and Japan. Japan’s response was to develop an inactivated tissue vaccine and to stop imports of live animals from China and Siberia. It finally eradicated the disease in 1922.

In the first World war, rinderpest spread from Asiatic Russia and sparked an epidemic in Poland and south-east Europe. The remnants of the epidemic were eliminated in Poland in 1921. 

A spectacular outbreak occurred in 1920 when a cargo of zebus from India en route for Brazil were disembarked at Antwerp in Belgium into dockside lairages to await the ship that was to take them across the Atlantic. The zebus were infected with rinderpest which they transmitted to in-contact American cattle that were distributed to Belgian farms. The zebus were embarked two days later for Brazil. Rinderpest broke out in Belgium and Brazil. The important sequel was the foundation of the Office Internationale des Epizooties (O.I.E.) in Paris as a world clearing-house on animal diseases data.

A second spectacular outbreak occurred in Australia in 1923. The origin was never established but suspicion fell upon pigs purchased as live provisions in Singapore. The ship then collected a cargo of cattle from a port in the Northern Territory of Australia which was disembarked at Freemantle. The surviving pigs were sold to a butcher. The outbreak was stamped out within days by slaughtering 3,000 cattle, pigs, sheep and goats.

Control measures in the early 1920s were still quarantine, no livestock movement, and slaughter and prophylaxis was limited to anti-serum alone or antiserum-virus immunisation. By 1925 every rinderpest laboratory was producing belatedly an inactivated vaccine. The original finder in 1902 was Dr. C. Kakizaki who published in Japanese and remained unheralded until 1918 (5). Production costs were high because cattle or buffaloes were needed as donors of infected tissues. Another snag was the slow build-up of the immunity which required booster doses. 

Meantime in India, Dr. J.T. Edwards obviated the major risk in the antiserum- virus simultaneous method of immunisation of transmitting other pathogens in the virulent virus inoculum. He passaged a bovine strain of rinderpest virus serially through goats to “fix” it and, fortuitously, produced a stable goat-adapted virus virulent for goats and attenuated for zebus (6). Simultaneous antiserum was not necessary. Moreover, one dose of goat-adapted vaccine inoculated into a yearling zebu protected it for life. The vaccine when dried by lyophilisation was thermo-stable and it revolutionized the control of rinderpest. In the 1940s Dr. R. Daubney predicted rinderpest could be eradicated through mass vaccination of national herds (7).

Goat-adapted rinderpest vaccine was far from being the ideal. Vaccinated animals exhibit post-vaccinal fevers that last for 4-5 days. Cattle, when febrile, are depressed, inappetent, tearful and rhinitic. The vaccine rarely kills but it immuno- suppreses, activating latent infections.

Dr. J. Nakamura visited the Indian Veterinary Research Institute at Mukteswar in the 1920s where he was impressed by Edwards’s ideas on passaging virus serially in a foreign host. When he returned to Korea he passaged the local strain of rinderpest virus serially in rabbits, goats being few in Korea. His Nakamura III strain was considered “fixed” after 600 passages and it proved to be more attenuated than Edwards’s goat vaccine (8). This lapinised vaccine was used first in Mongolia and later in China. Stockowners in Africa clamoured for the lapinised vaccine and it was used for two decades to protect highly susceptible cattle. Ironically, Nakamura’s lapinised vaccine proved to be too virulent for use in Korean Yellow and Japanese Black cattle. Further attenuation was achieved by serial passage in embryonated hen eggs.

Tentative steps at mass vaccination to control rinderpest were taken in China in the late 1940s and in equatorial Africa in the 1950s. India initiated a National Eradication Scheme in 1954 using goat-adapted vaccine. Over the first few years the success was remarkable; outbreaks fell from thousands per year to a few hundred per year. In the first 10 years, 117 million cattle and buffaloes were vaccinated out of a population of 132 million; as a result two-thirds of the country was freed from rinderpest. Seven years later, Dr. Ramachandran returned to India and played an important surveillant role detecting the presence of wild virus and rinderpest antibodies by application of his pen-side measles haemagglution test (9).

In 1952 an Inter-African Bureau for Epizootic Diseases was created by the Commission for Technical Cooperation in Africa, South of the Sahara specifically to study rinderpest. Dr. W.G. Beaton was the first Director and he initiated Joint Project 15 (JP 15) a multi-international vaccination campaign to rid Africa of rinderpest. JP 15 operated in the field between 1962 and 1976 in 22 African countries (10). In 1962, 17 countries had active rinderpest whereas in 1976 only two reported the disease. The first vaccine used was the goat-adapted vaccine until it was replaced by Dr. Plowright’s new cell-culture-adapted rinderpest virus vaccine in the 1960s (11). 

In 1980, a hidden low virulent virus focus in the Niger River sudd emerged and spread eastwards along the Sahel. Then, a virulent focus in southern Sudan erupted that spread rapidly westwards. One third of the cattle of the Fulani nation died; in Nigeria alone two million fell sick and half a million perished. The sequel was much worse because many herdsmen committed suicide. A less virulent virus reached Egypt in trade cattle meantime from the same focus in Sudan. It also spread south through Uganda in cattle looted by the victorious Tanzanian troops and ravaged the wildlife in Tanzania. 

The gains of JP 15 were tragically undone. These pandemics so alarmed the relatively new Heads of State to press OAU to launch a fresh campaign. In 1987 a fresh Pan-African Rinderpest Campaign (PARC) began field operations in 34 countries simultaneously. The mass vaccination phase was limited to two years and thereafter emphasis was on clinical and sero-surveillance.

In India a Task Force was appointed in 1983 to reassess the rinderpest situation having recognised that mass vaccination alone was not going to eradicate the disease. The country was classified into high, medium, low-risk, and rinderpest-free areas; each category was assigned a different strategy. For example, the use of vaccines was banned in low-risk and free areas. Instead, reliance was placed on intensive surveillance and prompt containment where necessary. 

In the 1970s FAO alongwith the International Atomic Energy Agency (IAEA) established veterinary diagnostic laboratories specifically in allegedly high risk countries in Africa and Asia. The objective was to identify the true prevalence of rinderpest. From 1980 FAO recruited three consultants to visit proven high risk countries (Fig.1) to prepare regional rinderpest campaigns by assessing real disease prevalences, diagnostic facilities, vaccine production plants, vaccine quality controls, available manpower and equipment, and estimates of budgets for the eradication of rinderpest. Their detailed report entitled “Global Eradication of Rinderpest” was presented, discussed and approved at a FAO Expert Consultation in Rome in October 1992 (12). The Expert Consultation issued a statement that global eradication of rinderpest was achievable by the year 2010. The 106th FAO Council authorised the Director-General to establish a priority programme the Emergency Prevention System for Transboundary Animal and Plant Pests and Diseases to be known by the acronym EMPRES. The initial focus was the Global Rinderpest Eradication Programme (GREP). The Secretariat collaborated with other international organizations such as OIE, IAEA, European Union and the Inter-African Bureau for Animal Resources (IBAR). The important link was OIE. It was asked to oversee the zoosanitary approach necessary to achieve eradication. They designed a practical moving pathway which every country had to follow culminating in a declaration of freedom from rinderpest virus (Fig. 2). 

Despite successful mass vaccinations in Africa, West Asia and South Asia in the 1980s, GREP was severely tested when launched at the end of 1994 by two novel epidemics. The first in 1993 was caused by a rare lineage II strain of the virus which is lethal in wildlife and avirulent in domesticated cattle, goats and sheep. The source was attributed to a group of refugee-owned cattle that crossed Kenya to northern Tanzania from Somalia. Mortality estimates exceeded 29,000 Cape buffaloes, 3,000 elands and 7,000 giraffes (13). The herds of smaller wild ruminants also declined. Cattle in contact with diseased wildlife were infected but had no clinical signs. FAO mounted an emergency vaccination programme in cattle in northern Tanzania and stopped the spread further south in 1997.

Figure 1 Regional Rinderpest Campaigns: 



PARC : Pan - African Campaign. WAREC : West Asia Campaign. SAREC : South Asia Campaign.

Figure 2 O.I.E. Eradication Pathway

The second novel epidemic was in naïve cattle and yaks in Pakistan in 1994 that was transported into Afghanistan in 1995. Losses were very high particularly among the yaks and their crosses. The numbers at risk were 500,000 of which 40,000 died (14). The source was the purchase of newly calved buffaloes from the Sind and Punjab Provinces to stock a new milk colony in Gilgit. The Afghanistan outbreak was also virulent in their local cattle. It was controlled by quarantine measures and vaccination of 150,000 cattle in 1996.

Several other minor rinderpest outbreaks occurred in 1994. Illegal cross-border movements of calves placed 1278 cattle at risk in Iran. Prompt destruction of the sick and vaccination of the rest removed the threat. Turkey also suffered from illegal movements of calves in 1994; 4283 animals were at risk but only 8 cases occurred, one of which died and the other 7 were destroyed. 

In 1995, in addition to the wildlife pandemic, rustled cattle were infected in Turkana, Kenya. There were 480 cattle in 13 herds but only 20 sickened of which 15 died. 

Turkey experienced a minor outbreak in 1996 in 24 young cattle which were slaughtered immediately. Confirmation of the diagnosis, however, was not achieved. In 1997, 10 out of 12 clinical cases died in Kajiado, Kenya. 

An outbreak in 1998 occurred in a village herd of 164 cattle in the Amur Region of Russia. It was totally unexpected because the Russian Federation was considered to be free of the disease. The diagnosis was confirmed but the source is still unknown. There were 70 clinical cases of which 43 died and 4 were killed for samples. The remaining cattle were re-vaccinated and remained healthy (15).

Rinderpest was not reported in 1999 but in 2000 the Manzoor Milk Colony at Karachi, Pakistan purchased 65 buffaloes up-country of which 3 were infected and one died. In 2001, 3,564 surveillance samples from cattle and buffaloes reared in the suspect areas of Pakistan were tested by two different serological methods; all were negative. The quarantine measures and restrictions were lifted in February 2001. 

Known endemic foci have been plotted in Africa, West Asia, South Asia and East Asia and they are encircled by cordon sanitaires of vaccinated animals. They pose a serious risk to the world cattle population. Their elimination depends on international action. For example, the Yemen is one of the last reservoirs of rinderpest and FAO/IAEA have responded to a request by the Government of Yemen to implement a project to eradicate the focus in 2002.

Other pockets of endemicity are southern Sudan and Somalia in Africa, the Kurdish Triangle and Saudi Arabia in West Asia, and Mongolia and Northern China in East Asia. 

GREP’s target is to stop routine rinderpest vaccination programmes in 2002 and to declare global provisional freedom from rinderpest in 2003.

References 

1. McDonald, J.M. (1942). Bull. Hist. Med., 12: 529.

2. Lancisi, G.M. (1715). Dissertationis historieae de bovilla peste. J.M. Salvioni, Rome.

3. Koch, A. (1891). Encyklopadie der gesammten Theirheil-kunde und Thierzucht. 8: 451. Verlag Moritz Perles, Wien und Leipzig.

4. Semmer, E. (1893). Berl. Tierärztl. Wschr., 23: 590

5. Kazaki, C. (1918). Kitasato Arch. Exp. Med., 2: 59.

6. Edwards J.T. (1928). Agric. J. India, 23: 185.

7. Daubney, R. (1947). Bull. Off. int. Epizoot., 28: 36.

8. Nakamura, J. and Kuroda, S. (1942). Jap. J. vet. Sci., 4: 75.

9. Ramachandran, S. and Scott, G.R. (1972). Indian vet. J., 49: 1060.

10. Lepissier, H.E. (1963). Bull. epizoot. Dis. Afr., 11 : 259.

11. Plowright, W. (1962). Bull. Off. int. Epizoot., 57 : 253.

12. Scott, G.R. and Provost, A. (1992). Global Eradication of Rinderpest. p. 109. FAO, Rome.

13. Kock, R.A. et al. (1999). Vet. Rec., 145 : 275.

14. Rossiter, P.B. et al. (1998). Vet. Rec., 143: 39.

15. Roeder, P. and Reichard, R. (1999). O.I.E. Mission to the Russian Federation concerning the Outbreak of Rinderpest in Amur Region in 1998. p. 18. O.I.E. FAO.

Authors Corresponding address:  

Sir Gordon . R. Scott

University of Edinburgh, Centre for Tropical Veterinary Medicine, Easter Bush, Roslin, Midlothian EH 25 9RG, Scottland, U.K.

The views expressed in this article are of the author(s), and any clarifications can be obtained from the author(s).