Origin of recent outbreaks of foot-and-mouth disease in North Africa, the Middle East and Europe. N.J. Knowles and P.R. Davies

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1 Origin of recent outbreaks of foot-and-mouth disease in North Africa, the Middle East and Europe N.J. Knowles and P.R. Davies Appendix 3 World Reference Laboratory for Foot-and-Mouth Disease, Institute for Animal Health, Pirbright Laboratory, Ash Road, Pirbright, Woking, Surrey, GU24 0NF, United Kingdom. Foot-and-mouth disease continues to be a threat to Europe despite its eradication from that continent by the end of the 1980 s. Since then sporadic outbreaks have occurred in 1991 (type O in Bulgaria), 1993 (type O in Bulgaria and Italy), 1994 (type O in Greece), 1996 (type O in Bulgaria and Greece and type A in Albania and the former Yugoslav Republic of Macedonia) and most recently in 2000 (type Asia 1 in Greece). Previous studies, using nucleotide sequence data, have shown that the type O outbreaks were introduced from the Middle East (Samuel et al., 1993; Knowles and Samuel, 1995) and the type A outbreaks came from the Indian sub-continent, possibly via Saudi Arabia (Knowles and Samuel, 1998). In the World Reference Laboratory for Foot-and-Mouth Disease (WRLFMD) we continue to monitor the movement of FMD virus strains around the world using phylogenetic analyses. The areas surrounding Europe present the greatest threat and we present here a brief report on the genetic characterization of FMD viruses isolated from recent outbreaks of type O in North Africa, type A in the Middle East and type Asia 1 in the Middle East and Greece. Foot-and-mouth disease type O in North Africa In February 1999 FMD type O was identified in Algeria. By March 1999, 158 premises and 139 of the country s 1,541 districts were affected. All cases were in cattle. In late February 1999 disease was found in cattle in the Oujda municipality of Morocco and in early March 1999 disease was detected in Tunisia, both in cattle and sheep. Full details may be found on the OIE Disease Information website ( The VP1 genes of representative virus isolates from all three countries were amplified by PCR and the products partially sequenced. Comparisons with sequences held on the WRLFMD database showed the North African viruses to have close relationships with viruses isolated in 1999 from Côte d Ivoire and Guinea (Fig. 1). A more distant relationship was found with a virus originating in Ghana in 1993 suggesting that this lineage is endemic in West Africa. Zebus smuggled into the south of Algeria in February were intercepted in the Sahara, south of El Bayadh and Bechar wilayas and in the south of El Oued wilaya, and were destroyed. These animals did not present clinical signs of FMD, but this indicates a possible route of entry for the disease. Previous epidemics of FMD type O affecting North Africa have been shown to originate from the Middle East (Samuel et al., 1999) as indicated in Fig. 2a.

2 Foot-and-mouth disease type A in the Middle East FMD type A is much less widespread than type O in the Middle East. However, previous studies have shown that new type A viruses may initially be recognized in Iran and subsequently spread westwards towards Europe (N.J. Knowles and A.R. Samuel, unpublished data). Monitoring of FMD type A viruses by nucleotide sequence analysis has shown three distinct genetic lineages to be present in Iran (Fig. 3). Figure 4 shows the Iranian and Turkish provinces from which we have received type A viruses between 1998 and The distribution of the three topotypes is indicted by shading. It is not clear where these virus ultimately originate since we receive few samples from Afghanistan and Pakistan. A more complete analysis of Indian type A strains is in progress in conjunction with the Indian Veterinary Research Institute at Mukteswar. Foot-and-mouth disease type Asia 1 in the Middle East and Greece In July 2000 FMD type Asia 1 was confirmed on six farms in the Evros region close to the border with Turkish Thrace. In early August 2000, three more farms were confirmed as being infected, two at Ferres (Evros region) and one at Potamia (Xanthi region). The latter outbreak was approximately 100 km from the Evros outbreaks. Prior to these outbreaks in Greece, FMD Asia 1 had been detected in Iran (1999) and Turkey ( ). Phylogenetic analysis of partial VP1 sequences show that viruses from all three countries were closely related (Fig. 5). They were also related to FMD Asia 1 viruses present in Pakistan (1998), India (1995) and Saudi Arabia (1994). Fig. 6 shows the conjectured spread of this recent Asia 1 strain. It was probably present in India prior to 1995 and spread to Saudi Arabia in However, the route of spread of Asia 1 to Greece in 2000 probably involved animals movements through Pakistan, Iran and Turkey. Previous outbreaks of Asia 1 have spread from the India subcontinent via Iran to Turkey (Firoozi Bandpay et al., 1974), however, the last outbreak of FMD Asia 1 in Greece in 1984 (Anon., 1984) was linked genetically to viruses occurring in Israel and Lebanon (Ansell et al., 1994). Conclusions FMD occurring in countries surrounding Europe may have originated in many parts of the world. In the past in North Africa FMD type O has originated for either the Middle East (Samuel et al., 1999) or West Africa (Fig. 1). It has been suggested that an A 24 -like found in Algeria and Morocco in 1977 originated from South America, while A 5 strains present in Libya and Tunisia in 1979 and Morocco in 1983 probably came from Europe (Beck and Strohmaier, 1987; Knowles et al., 1998). Many viruses occurring in the Middle East originate from the Indian subcontinent and enter either through the Gulf States or by an overland route via Afghanistan and Iran.

3 However, FMD viruses may enter the Middle East from Africa and even exotic serotypes such as SAT 1 and SAT 2 have occasionally caused epidemics. Routine molecular epidemiological studies are invaluable for monitoring the movement of FMD viruses and can detect the approach of novel strains before they reach Europe.

4 References Anonymous (1984). Greek outbreak in Thrace buffer zone. Bull. Off. Int. Epiz. 96: Ansell, D.M., Samuel, A.R., Carpenter, W.C. and Knowles, N.J. (1994). Genetic relationships between foot-and-mouth disease type Asia 1 viruses. Epidemiology and Infection 112: Beck, E. and Strohmaier, K. (1987). Subtyping of European foot-and-mouth disease virus strains by nucleotide sequence determination. Journal of Virology 61: Firoozi Bandpay, M.R., Amighi, M., Mastan, M.B. and Maleknejad, P. (1974). The outbreak of foot-and-mouth disease (Asia 1 type) in 1973 in Iran. Bull. Off. int. Epiz. 81: Knowles, N.J. and Samuel, A.R. (1995). Polymerase chain reaction amplification and cycle sequencing of the 1D (VP1) gene of foot-and-mouth disease viruses. Report of the Session of the Research Group of the Standing Technical Committee of the European Commission for the Control of Foot-and-Mouth Disease held jointly with the FMD Subgroup of the Scientific Veterinary Committee of the Commission of the European Community, Mödling, Vienna, Austria, September, 1994: Appendix 8: Knowles, N.J. and Samuel, A.R. (1998). Molecular techniques in foot-and-mouth disease epidemiology. Towards Livestock Disease Diagnosis and Control in the 21st Century: proceedings of an International Symposium on Diagnosis and Control of Livestock Diseases jointly organized by the International Atomic Energy Agency and the Food and Agriculture Organization of the United Nations, held in Vienna, 7-11 April Vienna: International Atomic Energy Agency, pp Knowles, N.J., Ansell, D.M. and Samuel, A.R. (1998). Molecular comparison of recent foot-and-mouth disease type A viruses from West Africa with historical and reference virus strains. Report of the session of the Research Group of the European Commission for the Control of Foot-and-Mouth Disease, Aldershot, United Kingdom, September Rome: FAO, Appendix 4: Samuel, A.R., Ansell, D.M., Rendle, R.T., Armstrong, R.M., Davidson, F.L., Knowles, N.J. and Kitching, R.P. (1993). Field and laboratory analysis of an outbreak of foot-andmouth disease in Bulgaria in Revue scientifique et technique de l'office International des Epizooties 12: Samuel, A.R., Knowles, N.J. and Mackay, D.K.J. (1999). Genetic analysis of type O viruses responsible for epidemics of foot-and-mouth disease in North Africa. Epidemiology and Infection 122:

5 ALG = Algeria BAR = Bahrain BHU = Bhutan CIV = Cote d'ivoire ERI = Eritrea ETH = Ethiopia GHA = Ghana GNA = Guinea IRN = Iran IRQ = Iraq ISR = Israel JOR = Jordan LEB = Lebanon KUW = Kuwait MOR = Morocco PAK = Pakistan QTR = Qatar SAU = Saudi Arabia TUN = Tunisia TUR = Turkey UAE = United Arab Emirates YEM = Yemen West Africa ME-SA Euro-SA O/ALG/1/99 O/ALG/2/99 O/ALG/3/99 O/MOR/2/99 O/MOR/11/99 O/CIV/8/99 O/GNA/6/99 O/GNA/10/99 O/TUN/1/99 O/TUN/5/99 O/GHA/5/93 O/GHA/9/93 O/BAR/2/97 O/IRN/5/97 O/KUW/3/97 O/KUW/4/97 O/UAE/7/97 O/IRN/15/97 O/IRN/16/97 O/ISR/1/96 O/SAU/2/95 O/SAU/5/95 O/SAU/14/95 O/SAU/20/95 O/SAU/28/95 O/YEM/8/95 O/KUW/1/96 O/JOR/3/96 O/LEB/1/98 O/LEB/3/98 O/SAU/2/97 O/KUW/1/98 O/BAR/8/98 O/IRN/20/98 O/IRN/8/99 O/IRN/12/98 O/IRN/1/99 O/BHU/1/98 O/BHU/2/98 O/BHU/6/98 O/ISR/2/99 O/ISR/3/99 O/ISR/5/99 O/LEB/9/98 O/LEB/12/98 O/LEB/14/98 O/LEB/17/98 O/SAU/36/98 O/SAU/38/98 O/SAU/41/98 O/SAU/25/98 O/YEM/3/98 O/YEM/6/98 O/SAU/1/99 O/SAU/2/99 O/ISR/A/99 O/YEM/15/98 O/IRQ/2/99 O/IRQ/9/99 O/QTR/3/99 O/IRN/8/94 O/IRN/8/95 O/IRN/13/95 O/IRN/27/95 O/IRN/10/95 O1/Manisa/69 O/PAK/1/98 O/ERI/1/96 O/ETH/8/94 O/YEM/4/95 O1/Kaufbeuren/ Percentage nucleotide difference (nt of VP1) Fig. 1. Foot-and-mouth disease type O epidemic in North Africa in MOROCCO TUNISIA & 1994 MOROCCO 1999 TUNISIA WESTERN SAHARA ALGERIA LIBYA EGYPT WESTERN SAHARA ALGERIA LIBYA EGYPT MAURITANIA MALI NIGER ERITREA CHAD SENEGAL SUDAN THE GAMBIA DJIBOUTI BURKINA -BISSAU TOGO NIGERIA ETHIOPIA SIERRA-LEONE COTE CENTRAL D'IVOIRE BENIN GHANA AFRICAN REPUBLIC LIBERIA CAMEROON UGANDA SOMALIA EQUATORIAL KENYA GABON RWANDA CONGO ZAIRE BURUNDI MAURITANIA MALI NIGER ERITREA CHAD SENEGAL SUDAN THE GAMBIA DJIBOUTI BURKINA -BISSAU TOGO NIGERIA ETHIOPIA SIERRA-LEONE COTE CENTRAL D'IVOIRE BENIN GHANA AFRICAN REPUBLIC LIBERIA CAMEROON UGANDA SOMALIA EQUATORIAL KENYA GABON RWANDA CONGO ZAIRE BURUNDI TANZANIA TANZANIA a) b) ZAMBIA ZIMBABWE MALAWI MOZAMBIQUE MADAGASCAR ZAMBIA ZIMBABWE MALAWI MOZAMBIQUE MADAGASCAR NAMIBIA BOTSWANA NAMIBIA BOTSWANA SWAZILAND SWAZILAND SOUTH AFRICA LESOTHO SOUTH AFRICA LESOTHO Fig. 2. The origin of foot-and-mouth disease type O epidemics in North Africa between 1989 and 1999.

6 ALB, Albania BRA, Brazil FRA, France HOL, Holland IND, India IRN, Iran IRQ, Iraq MCD, Macedonia SAU, Saudi Arabia TUR, Turkey A/ALB/1/96 A/ALB/4/96 A/MCD/1/96 A/MCD/3/96 A/MCD/5/96 A/MCD/6/96 A/MCD/8/96 A/ALB/3/96 A/IND/300/94 A/SAU/16/95 A/SAU/19/95 A22/IND/17/77 VS A22/IRQ/24/64 A22/Mahmatli/TUR/65 A/SAU/104/93 (P16) A/SAU/111/93 (P21) A/IRN/4/2000 A/IRN/7/2000 A/IRN/8/2000 A/IRN/10/2000 A/IRN/1/94 A/IRN/19/95 A/IRN/87 A/SAU/29/93 A/SAU/99/93 (P14) A/TUR/9/91 A/TUR/1/92 A/TUR/3/92 A/TUR/14/91 A/TUR/12/91 A/TUR/3/95 A/TUR/8/96 A/TUR/16/96 A/TUR/11/97 A/IRN/22/99 A/TUR/6/99 A/TUR/4/99 A/IRN/1/96 A/IRN/7/96 A/IRN/3/96 A/IRN/11/96 A/IRN/17/96 A/IRN/1/97 A/TUR/12/97 A/TUR/1/98 A/TUR/2/98 A/TUR/14/98 A/TUR/21/98 A/TUR/23/98 A/TUR/25/98 A/TUR/27/98 A/TUR/32/98 A/TUR/17/98 A/IRN/1/98 A/IRN/3/98 A/IRN/4/98 A/TUR/4/98 A/IRN/28/99 A/IRQ/17/2000 A/TUR/4/2000 A/TUR/1/2000 A/TUR/5/99 A24/Cruzeiro/BRA/55 A5/Allier/FRA/60 A10/HOL/42 Indian/Middle Eastern (A22) topotype Turkish topotype Iran-99 topotype Iran-96 topotype European/South American topotype Percentage nucleotide difference (nt of VP1) Fig. 3. Relationships between various FMD type A viruses and recent isolates from Iran, Iraq and Turkey Kowcaeli Sakarya Artvin Kutahya Aydin Burdur Ankara Tokat Malatya Erzincan Kars W. Azerbaijan E. Azerbaijan Gilan Markazi Qom Qazvin Khorasan Topotype Iran-96 Iran-99 Iran-96 & Iran-99 Fars India / Middle East (A22 -like) not done Fig. 4. Foot-and-mouth disease type A topotypes present in Turkey and Iran between 1998 and 2000

7 14.3% AFG, Afghanistan BAN, Bangladesh BAR, Bahrain BHU, Bhutan GRE, Greece IND, India IRN, Iran ISR, Israel LAO, Laos LEB, Lebanon NEP, Nepal PAK, Pakistan SAU, Saudi Arabia TAI, Thailand TUR, Turkey YEM, Yemen AFG/4/71 BAN/30/79 SAU/2/80 SAU/11/85 TUR/15/73 BAN/13/78 BAN/1/79 BAN/1/87 BHU/1/86 NEP/23/85 WBN/IND/117/85 NEP/19/86 (1985) IND/9/89 (1988) NEP/8/87 NEP/36/87 NEP/58/88 NEP/28/90 (1989) HKN/20/80 YEM/15/79 YEM/2/80 (1979) IND/8/79 IND/91/79 SAU/48/91 SAU/9/92 SAU/10/92 SAU/32/92 IND/10/82 IND/60/79 IND/5/89 (1988) IND/A/93 (Mandya Karnataka) GRE/2/2000 IRN/58/99 TUR/6/2000 TUR/8/99 TUR/3/2000 TUR/10/99 IND/233/95 IND/26/95 IND/40/95 IND/43/95 SAU/39/94 SAU/40/94 PAK/3/98 IND/51/95 PAK/2/98 BAR/1/85 GRE/1/84 ISR/3/89 LEB/3/83 LEB/1/84 N1214/Armenia/USSR/84 N1181/Azerbaijan/USSR/83 ISR/1/84 IND/63/72 MukVS PAK/1/85 PAK/4/69 PAK/1/71 PAK/1/74 PAK/2/76 (1975) PAK/1/54 Bangkok/TAI/ Percentage nucleotide difference (nt of VP1) Fig. 5. Comparison of recent FMD type Asia 1 viruses from Iran, Turkey and Greece. Greece Turkey ( ) (July 2000) Iran (1999) Saudi Arabia (1994) Pakistan (1998) India (1995) Fig. 6. The likely recent spread of FMDV-Asia1