Contagious Bovine Pleuropneumonia: A Passage to India: History
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Robin A. J. Nicholas

The World Organization for Animal Health (WOAH)-listed contagious bovine pleuropneumonia (CBPP) emerged first in Europe and then spread to Eastern Asia, including Japan and China, from the Northern Territories of Australia at the end of the 19th century. Its route to India, however, is less well known as there is little evidence for large importations of cattle from Australia. The lack of accurate diagnostic tests at this time meant veterinary authorities relied solely on clinical and pathological signs, many of which were non-specific. Consequently, any diagnoses of CBPP reported in the early 20th century must be viewed with caution. More convincing reports of CBPP confirmed by laboratory tests were made in the 1930s and 1940s in the Indian state of Assam. Eradication campaigns began in the 1940s with immunizations of live attenuated vaccines and then more comprehensively in the 1950s and 1960s, supplemented with serological screening and the establishment of quarantine centres at international borders. 

  • CBPP
  • cattle
  • Assam

1. Introduction

Contagious bovine pleuropneumonia (CBPP), commonly known as “lung sick”, once a scourge of cattle worldwide, is now restricted to about 25 countries in sub-Saharan Africa with Ethiopia, Ghana, Tanzania and Angola having the highest prevalence [1]. Very recently, though unofficial, reports have indicated it may also be present in the Punjab region of Pakistan. The true economic and social impact of CBPP is unknown because rigorous surveillance is not routinely carried out in all African countries. Today, for the most part, CBPP is an enzootic disease with occasional serious outbreaks but it still takes a toll on cattle, resulting in losses due to poor growth rates, fertility, emaciation and a shortage of draft animals [2].
The characteristics of CBPP and the history of its worldwide spread has been well documented [2][3][4][5]. While it is not possible to completely exclude a CBPP-like disease in classical Roman times, it seems highly speculative given the lack of laboratory diagnosis and knowledge of disease pathology at the time. Descriptions of CBPP-like clinical signs were reported by Virgil but seems to have had a much wider host range, including dogs and birds, than seen today [3]. Furthermore, his descriptions of cattle vomiting blood and froth does not seem much like CBPP. The consensus, backed by molecular studies [5], is that this disease, known then as “pulmona,” first appeared in Middle Europe in the 16th century and was differentiated from other respiratory diseases by Bourgelat in 1765 [2]. It spread by wars and trade during the early 19th century throughout the continent, predominantly by movements of the favoured Swiss and Dutch cattle. The Netherlands became a hot bed of infection with high mortality and morbidity rates. Britain too became infected through the importation of cattle from mainland Europe, resulting in huge losses. CBPP was then exported from Britain and the Netherlands via infected cattle to the USA/Australia and South Africa, respectively. From the latter, CBPP-affected cattle were trekked north by Boer farmers [6] and/or British troops [7], initially into East Africa and then via other cattle movements into the rest of Africa. One hypothesis says that CBPP may have been introduced even earlier to Africa also by the British during a military expedition in 1868 into Abyssinia, now present-day Ethiopia [2]. Another theory suggests that it may already have been present in Africa, as the European explorer Thompson reported Masai cattle dying of a disease with signs similar to CBPP [6]. Though not mutually exclusive, Dupuy et al. [5] ingeniously suggested another possible route of transmission: via cattle from the Portuguese bases along the west African coast, possibly as early as the 17th century. However, the evidence for this speculation comes from molecular typing of the causative agent, Mycoplasma mycoides subsp. mycoides, which showed three separate genotypes in central, eastern and western Africa [8]. Unfortunately, the number of strains available was too few to provide a truly accurate assessment of the epidemiology of CBPP in Africa.
Various control measures including slaughter, quarantine, movement restrictions and vaccination led eventually to its eradication first in the USA in 1892, then Britain at the end of the 19th century, Australia in the 1960s, China in the 1980s and the whole of Europe by the end of the 20th century. Other countries, including India and Pakistan, reported their last cases in 1990 and 1997, respectively [9].

2. India

The exact date of arrival of CBPP in India has been hotly disputed and varies from the late 19th century to the early 1940s. A perusal of the Provincial Civil Veterinary Department’s annual reports by Gopalakrishnan [10] indicated that the opinion up to the late 1930s was always divided as to the existence of the disease in India. The earlier proposal by Windsor that the horn of Africa was infected during a British military operation which began in India is clearly unlikely, as CBPP had almost certainly not reached India at the time of the expedition in 1868. Furthermore donkeys, not bullocks, were the main beasts of burden for the invasion of Abyssinia [11]. Furthermore, there does not seem to have been any reports of major imports of cattle from Australia around this time, as trade did not begin for another 20 years [12]. Indeed, had there been any importation of infected cattle to India in the late 19th and early 20th centuries then there would almost certainly have been reports of explosive and prolonged outbreaks in the immunologically naïve local herds such as that seen in Australia and Southern Africa [4].
This is not to say that there were not major outbreaks of respiratory diseases in Indian cattle during the late period of British colonization. From 1892–1893, CBPP was included by the veterinary authorities in an annual list of diseases believed to occur in India, although any diagnosis at that time would have been based solely on clinical and pathological signs. In the following decade, thousands of cattle died with lesions thought to be CBPP. From 1894–1895, the superintendent of South Punjab reported an outbreak of “pleuropneumonia” in the Ferozepore area, comprising 138,000 cattle of which 4000 died. Similar diseases were recorded in the remarkably detailed annual reports of the Civil Veterinary Department between 1893 and 1904 in the same province, affecting 140,636 animals of which 5631 died. However, there were doubts expressed by some authorities at the time, including those in Bengal, that this was not true CBPP and, with hindsight, was most likely bovine haemorrhagic septicaemia caused by Pasteurella multocida. Indeed, the veterinary superintendent at the time stated the following: “It was much more likely that these were ordinary pneumonias with pleurisy” [13].
Identification of diseases, particularly multifactorial respiratory conditions in cattle in the late 19th century, was not an exact science, as seen with a transatlantic trade dispute between the USA and Great Britain. An argument had broken out over the on-going diagnoses “…of the insidious lung disease pleuropneumonia” in cattle imported from the USA in 1879 [14]. Despite the irony of Britain having exported CBPP to the USA in the early half of the 19th century and at the time being heavily affected itself, British veterinary officials wanted to slaughter cattle imported from the USA that were diagnosed as being affected with CBPP. However, these diagnoses were contested by both the US authorities and some experts in Britain who believed it was a general non-contagious and less fatal bronchitis, known today as “shipping fever”, which had developed during a stressful transatlantic voyage. While never satisfactorily resolved, the dispute accelerated US attempts to eradicate CBPP, which it did in 1892. Britain suffered for a few years more.
In India, in the early part of the 20th century, sporadic reports of a CBPP-like disease were made near Karachi, the United Provinces, Berar, Jubbulpore and Nagpor districts with high mortality, although once again, CBPP could not confirmed. One convincing reason that these diseases may have been misdiagnosed was that there were few further reports of CBPP between 1905 and 1929, but instead, a new category was inserted into the records, namely haemorrhagic septicaemia, suggesting doubts in the earlier diagnoses. As is well known, CBPP does not disappear so suddenly following 10 years of infection without severe control measures being put in place for which there was no evidence in India. The reasons for these doubts must have been due to staff inexperienced at differentiating the various bovine pneumonias and the uncertainty of disease nomenclature at the time, compounded by the huge distances and difficulties encountered by veterinarians examining diseased cattle in the field.
Further arguments for the absence of CBPP up to that time came from two senior veterinary officers serving in India in the early 20th century. J.T.Edwards in 1927 said that “…India…for some reason has escaped infection” [13]; 12 years later, Shirlaw [13] stated, in no uncertain terms after viewing reports dating back to the beginning of that century, that “There is no evidence that CBPP existed or has ever existed in British India”. While Shirlaw was probably correct about the historic reports, he believed that many of the later reports of a CBPP-like disease in Assam, an isolated state in northeast India bordered by Bangladesh, Myanmar, Bhutan and China (Figure 1), were caused, based on culture and histopathology, by a fungal pathogen. The mycotic-looking Borrelomyces peripneumoniae, later to be known as the bacterium Asterococcus mycoides then renamed Mycoplasma mycoides, the definitive causative agent of CBPP, was later identified from the pleural fluid of affected cattle. Five years after his pronouncement of its non-occurrence in India, Shirlaw had to admit that his fungal disease was in fact true CBPP and ravaging cattle in Assam [15]. He and his co-workers at the Imperial Veterinary Research Institute, Izatnagar, Uttar Pradesh were able to develop “a medium of choice” for the in vitro culture of the “Assam bovine pleuropneumonia organism” and showed that strains from this province were immunologically similar to confirmed CBPP pathogens from East Africa and Australia. It is interesting to note that despite taking 3 and 10 weeks to arrive from Kenya and Australia, respectively, the strains could be revived satisfactorily in the newly developed broth and still retained pathogenicity in cattle.
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Figure 1. Location of the Indian state of Assam (in red) with its neighbours.

This entry is adapted from the peer-reviewed paper 10.3390/ani13132151

References

  1. World Organization for Animal Health (WOAH). Annual Report. Paris, OIE. Available online: https://www.oie.int/scientific-expertise/reference-laboratories/annual-reports/ (accessed on 5 March 2023).
  2. Provost, A.; Perreau, P.; Bréard, A.; Le Goff, C.; Martel, J.L.; Cottew, G.S. Contagious bovine pleuropneumonia. Rev. Sci. Tech. Off. Int. Epizoot. 1987, 6, 625–679.
  3. Blancou, J. Early methods of surveillance and control for contagious bovine pleuropneumonia. Rev. Sci. Tech. Int. Off. Epizoot. 1996, 15, 1263–1282.
  4. Egwu, G.; Nicholas, R.A.J.; Ameh, J.A.; Bashiruddin, J.B. Contagious bovine pleuropneumonia: An update. Vet. Bull. 1996, 66, 195–208.
  5. Dupuy, V.; Manso-Silván, L.; Barbe, V.; Thebault, P.; Dordet-Frisoni, E.; Citti, C.; Poumarat, F.; Blanchard, A.; Breton, M.; Sirand-Pugnet, P.; et al. Evolutionary history of contagious bovine pleuropneumonia using next generation sequencing of Mycoplasma mycoides subsp. mycoides “Small Colony”. PLoS ONE 2012, 7, e46821.
  6. Davies, G. Contagious bovine pleuropneumonia: What every veterinarian ought to know. State Vet. J. 1991, 1, 9–11.
  7. Tambi, N.E.; Maina, W.O.; Ndl, C. An estimation of the economic impact of contagious bovine pleuropneumonia in Africa. Rev. Sci. Tech. Off. Int. Epizoot. 2006, 25, 999–1011.
  8. Yaya, A.; Manso-Sylvan, L.; Blanchard, A.; Thiaucourt, F. Genotyping of Mycoplasma mycoides subsp. mycoides SC by multilocus sequence analysis allows molecular epidemiology of contagious bovine pleuropneumonia. Vet. Res. 2008, 39, 1–9.
  9. OIE. World Animal Health in 2012; World Organisation for Animal Health: Paris, France, 2013.
  10. Gopalakrishnan, V.R. Preliminary note on vaccination against bovine contagious pleuropneumonia in Assam. Indian J. Vet. Sci. Anim. Husb. 1946, 16, 209–210.
  11. Nicholas, R.A.J. Contagious bovine pleuropneumonia: In search of the origins and virulence of lung sickness. Microbiologist 2009, 10, 41–43.
  12. Anon. Industry History-Australian Livestock Exporters’ Council (ALEC). Available online: https://www.auslivestockexport.com (accessed on 14 March 2023).
  13. Shirlaw, J.F. Observations on the existence of contagious bovine pleuropneumonia in British India. Indian J. Vet. Sci. Anim. Husb. 1939, 9, 139–150.
  14. Kastner, J.; Powell, D.; Crowley, T.; Huff, K. Scientific conviction amidst scientific controversy in the transatlantic livestock and meat trade. Endeavour 2005, 29, 78–83.
  15. Shirlaw, J.F.; Iver, P.R.K. Studies on contagious bovine pleuropneumonia in Assam. Indian J. Vet. Sci. Anim. Husb. 1946, 16, 191–208.
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