T. RUFAEL, A. CATLEY, A. BOGALE, M. SAHLE AND Y. SHIFERAW

The Global control of FMD - Tools, ideas and ideals – Erice, Italy 14-17 October 2008

Appendix 62

PARTICIPATORY EPIDEMIOLOGY AS COMPARED TO CONVENTIONAL FOOT AND MOUTH DISEASE SURVEILLANCE TOOL

T. Rufael

1*, A. Catley2, A. Bogale

3, M. Sahle

1 and Y. Shiferaw4

1National Animal Health Diagnostic and investigation Center, Ethiopian, P.O. Box 04, Sebeta, Ethiopia e-mail: rufaelc@yahoo.com

2Feinstein International Center, Friedman School of Nutrition Science and Policy, Tufts University, P.O. Box 1078, Addis Ababa

3Faculty of Veterinary Medicine, Addis Ababa University, P.O. Box 34, Debre Zeit

4Ethiopian Institute of Agricultural Research, P.O. Box 2003, Addis Ababa

ABSTRACT

Participatory epidemiology (PE) was used on the Borana plateau of southern Ethiopia to understand pastoralist’s perceptions of the clinical and epidemiological features of foot-and-mouth disease (FMD) in cattle. This paper describes the use of Participatory epidemiology to collect information on the basic epidemiology of FMD and compare the data from Participatory epidemiology with estimate of conventional seroprevalence result of FMD in Borana pastoral herds. Participatory appraisal and conventional veterinary investigation methods were applied to generate information on FMD in Borana pastoral system. The participatory appraisal methods used were Matrix scoring, Clinical observation, Proportional piling, and Seasonal calendar. The validity of participatory diagnosis of disease and their perceptions of proportions of animal affected by FMD can be cross checked by modern laboratory diagnosis. Serum samples were collected from randomly selected Borana cattle herds and screening by 3ABC ELISA for Non structural protein. Positive serum samples were serotyped for specific FMDV using liquid phase blocking ELISA (Hamblin et al, 1986a, b). Matrix scoring showed good agreement between informant groups on the clinical signs of acute and chronic FMD, and findings were cross-checked by clinical examination of cattle and assessment of previous clinical FMD at herd level by detection of antibody to non structural proteins of FMD virus. The positive predictive value of pastoralist’s diagnosis of FMD at herd level was 93.1%. The annual age-specific incidence and mortality of acute FMD in 50 herds was estimated using proportional piling. The estimated mean incidence of acute FMD varied from 18.5% in cattle less than two years of age to 14.0% in cattle three to four years of age. The estimated mean mortality due to acute FMD varied from 2.8% in cattle less than two years of age to 0.3% in cattle three of age or older. Pearson correlation coefficients for acute FMD by age group were −0.12 (p>0.05) for incidence and −0.59 (p<0.001) for mortality. Estimates of the annual incidence of chronic FMD varied from 0.2% in cattle less than two years of age to 1.8% in cattle three to four years of age. The Pearson correlation coefficient for the incidence of chronic FMD by age group was 0.47 (p<0.001). Outbreaks of FMD peaked in Borana cattle during the two dry seasons and were attributed to increased cattle movement to dry season grazing areas. The mean seroprevalence of FMD was estimated at 21% (n=920) and 55.2% of herds (n=116) tested seropositive. Serotyping of 120 seropositive samples indicated serotypes O (99.2%), A (95.8%), SAT 2 (80%) and C (67.5%). The observed agreement between pastoralist perception on FMD diagnosis and conventional laboratory diagnosis from this study has proven that Borana pastoralists have an enormous wealth of knowledge on diagnosis of cattle diseases. Therefore, Participatory Appraisal methods complements FMD surveillance to gain better understanding of FMD dynamics in pastoral areas and help to formulate appropriate disease control strategies.

1. INTRODUCTION

Foot-and-mouth disease (FMD) is highly contagious viral disease of cloven-hoofed domestic and wild animals. It is widely distributed and occurs most commonly in Asia, Africa, the Middle East, and parts of South America (Kitching 1999). In pastoral areas of Africa outbreaks of FMD are reported frequently but the disease remains largely uncontrolled using conventional methods (Thomson and Bastos 2005). Providing veterinary services to the communities according to the western model has proven difficult due to lack of infrastructure and the veterinarian has limited

The Global control of FMD- Tools, ideas and ideals – Erice, Italy 14-17 October 2008

2. METHODOLOGY

The research was conducted in three districts (Yabello, Dirre and Moyale) of Borana pastoral system of Oromia Regional State, located between 03037' 23.8" to 050 02' 52.4" North and 370 56' 49.4" to 390 01' 10.1"East, in the Southern part of Ethiopia. The Borana pastoral system represents a vast lowland area, covering about 95,000 km2 (Coppok, 1994) and bordering northern Kenya. Borana pastoralists are mainly cattle-keepers and they manage their cattle using traditional pastoral systems. The methodology involved both participatory appraisal and conventional veterinary investigation methods were applied to generate information on FMD in the study areas. The participatory appraisal methods used were Matrix scoring, Clinical observation, Proportional piling, and Seasonal calendar was adapted from method described by Catley, (Catley, 2005; Catley et al., 2001). The validity of participatory diagnosis of disease and their perceptions of proportions of animal affected by FMD can be cross checked by modern laboratory by using antibody detection. 920 Serum samples were collected from randomly selected Borana cattle herds and examined for antibodies to 3ABC non structural proteins of FMD virus by using 3ABC ELISA (chekit-FMD 3ABC, Intervet). 120 Samples, 3ABC ELISA positive samples were further tested to determine FMD virus serotypes O, A, C and SAT2 by using the liquid phase blocking ELISA according to the manufacturers manual (Ferris, 2004).

3. RESULTS

The results of matrix scoring for FMD and other diseases are shown in Table 1. There was good agreement between the 12 informant groups for all 17 disease indicators (W=0.54 to 0.96; p<0.001). In all the informants groups the informants scored FMD by considering both acute and chronic forms of the disease called hoyaale and gaandile respectively. Hoyaale was associated with salivation, lameness, skin lesions, reduced appetite, abortion, decreased milk yield, loss of body condition and mortality (in young animals). In comparison, gaandile affected animals that recovered from hoyaale but later developed signs of hair overgrowth, panting, shade-seeking behaviour and infertility. Informants also mentioned that if these cases produced calves, the calves were weak or stillborn and the dam’s milk was watery for the first two week. Matrix scoring also indicated that hoyaale/FMD was transmitted by direct contact and affected wildlife such as oryx,

experience in harsh environments of pastoral system. Participatory Appraisals (PA) is a systematic collection and analysis of data for diseases like FMD that are often under reported by conventional veterinary services due to comparatively high tolerance of local breeds to the clinical episodes of the disease (Leforban, 2005), However, at certain times of year pastoralists rely heavily on milk for food and therefore, they often prioritize FMD due to its impact on milk supply. They also associate FMD with mortality in calves and ‘chronic FMD’ cases showing heat intolerance, reduced fertility and other signs (Catley et al. 2004). Participatory epidemiology is the application of participatory methods in a number of animal health epidemiological disease surveillance. The participatory methods offer input in addition to laboratory based epidemiology, that pastoralists often possess detailed indigenous knowledge on livestock diseases and in terms of clinical diagnosis, describe diseases in similar ways to veterinarians (Catley, 2006). Veterinarians and livestock workers have used and are presently using a variety of PA methods to investigate animal health problems (Catley, 1999). The tools include interviewing, scoring and ranking, and visualization such as seasonal calendars, maps, Venn diagrams, and flow charts. Although PE studies can be purely qualitative in nature, standardization and repetition of PE methods can produce quantitative data leading to estimates of disease incidence, mortality or other variables. The process of triangulation in Participatory epidemiology is used to improve the validity of findings and involves cross checking information from different sources or methods, including conventional veterinary methods. The global rinderpest eradication program adopted Participatory epidemiology as a surveillance tool for controlling rinderpest. This approach was subsequently used in both rural and urban settings in Africa and Asia, for foot-and-mouth disease, peste des petitis ruminantus and highly pathogenic avian influenza (Jost et. al, 2007). Participatory disease surveillance approach is now recognized in world organization for animal health (OIE) guidelines for rinderpest surveillance and as an important approach for general surveillance (OIE, 2007). This paper describes the use of Participatory epidemiology to collect quantitative and qualitative information on the basic epidemiology of FMD and compare the data from Participatory epidemiology with estimate of conventional seroprevalence result of FMD in Borana pastoral herds.

The Global control of FMD - Tools, ideas and ideals – Erice, Italy 14-17 October 2008 kudu, and gazelle. Informants noted that other domestic animals such as sheep and goats could also suffer from hoyaale/FMD. Eight chronic FMD (gaandile) case identified by pastoralists were examined clinically by researcher for the triangulation. Table 1: Summarized Matrix scoring of disease indicators in three districts of Borana pastoral area (Dec. 2004-Nov. 2005).

Indictors Coughing (W=0.956***) Salivation (W=0.885***) Abortion W=0.881***) Lameness (W=0.900***) Mortality (W=0.871***) Reduced milk production (W=0.543***) Loss of body weight (W=0.814***) Skin lesion (W=0.782***) Teat lesion (W=0.762***) Hair over growth (W=0.902***) Panting (W=0.778***) Seek shade (W=0.768***) Decrease fertility W(=0.840***) Decrease market value (W=0.624***) Disease affect wild life (W=0.569***) Transmitted by tick (W=0.9245***) Transmitted with contact (W=0.840***) CBPP (Sombesa) FMD (Hooyale) LSD (Suuki) Black leg (Haarka)

Mastitis (Nakarsa) 25(17-25) 0(0-8) 0(0-0) 0(0-0) 0(0-0) 0(0-6) 25(15-25) 0(0-0) 0(0-0) 0(0-0) 0(0-7) 25((18-25) 0(0-7) 0(0-2) 0(0-0) 0(0-3) 13.5(6-24) 0(0-3) 7.5(1-13) 0(0-7) 7.5(3-11) 3(0-5) 4(0-6) 10.5(7-22) 0(0-6) 0(0-8) 11(6-18) 3(0-9) 0(0-8) 10(2-13)

1(0-8) 16(8-25) 6(0-12) 0(0-2) 0(0-4)

0(0-0) 7(0-10) 15.5(1215)

0(0-5) 2(0-8) 0(0-0) 0(0-5) 5(0-17) 0(0-0) 19.5(825) 0(0-0) 25(17-25) 0(0-8) 0(0-0) 0(0-0)

3(0-15) 22(10-25) 0(0-5) 0(0-2) 0(0-0) 0(0-10) 20.5(14-25) 0(0-5) 0(0-4) 0(0-0) 0(0-0) 22(14-25) 2.5(0-11) 0(0-0) 0(0-0)

0(0-9) 9(6-12) 7.5(4-13) 0(0-0) 5(0-13)

0(0-0) 19(0-25) 0(0-7) 0(0-14) 0(0-5)

0(0-0) 0(0-0) 0(0-12) 0(0-0) 25(13-25)

4.8(2-8) 6(5-10) 7(4-10) 0.5(0-4) 0(0-2)

Number of informants groups =12; W = Kendall’s Coefficient of Concordance (*P<0.05; **P<0.01; ***P<0.001). W values vary from 0 to1; the higher the value the higher the level of agreement between informants groups. The number out of parentheses indicates median scores of the 12 groups and minimum and maximum limits are shown in Parentheses. Age-specific incidence and mortality of acute FMD (hoyaale) is shown in Fig 1. Pearson correlation coefficients for incidence and mortality by age group were −0.12 (p>0.05) and -0.59 (p<0.001) respectively. The Pearson correlation coefficient for incidence caused by chronic FMD (gaandile) by age group was 0.47 (p<0.001).

The Global control of FMD- Tools, ideas and ideals – Erice, Italy 14-17 October 2008 Mean incidance and mortality of acute FMD and 95% C I

30

20

10

0

-10

Calves Weaner Young Adult I (r= -0.12,p=0.08)

M (r= -0.59,p=0.00)

Figure 1: The mean annual incidence and mortality of acute FMD in different age groups of cattle in Borana pastoral area (Dec. 2004-Nov. 2005)

A summarized seasonal calendar for livestock diseases, rainfall, tick infestation, cattle movement, and contact with wildlife is shown in Table 2. Moderate to good agreement (W=0.29 to 0.99) was evident between informant groups for the diseases CBPP (sombessa), acute FMD (hoyaale), LSD (sukii), blackleg (haarka) and mastitis (nakarsa), and also for seasonal rainfall and cattle movement. The incidence of acute FMD (hoyaale) peaked during the two dry seasons called short dry season (adoolessa) and long dry season (bona), with relatively higher incidence in the main dry season. Cattle movement followed a similar seasonal pattern to the incidence of acute FMD. Table 2: Summarized seasonal calendar on the occurrence of different diseases of cattle in Borana pastoral area (Dec. 2004-Nov. 2005)

Borana seasons Gana (Long rain) Adoolessa ( Cold dry) Hagayya (Short rain) Bona (Long dry)

53.1.1.1.1.1.1.1 Months by Gregorian calendar M A M J J A S O N D J F Rainfall (W=0.995)*** 12(10-13) 2(0-3) 6(4-8) 0(0-2)

CBPP (Sombesa) (W=0.700)*** FMD (Hooyale) (W=0.938)*** 2(0-5) 5.5(2-8) 1.5(0-4 ) 10(3-13)

1(0-3) 5(4-7) 1(0-3) 12.5(10-16)

LSD (Suuki) (W=0.870)*** Blackleg (Haarka) (W=0.919)*** 3(1-5) 12.5(9-18) 4(0-6) 0(0-2)

13.5(9-18) 2(0-3) 4(0-8) 0(0-1)

The Global control of FMD - Tools, ideas and ideals – Erice, Italy 14-17 October 2008

Mastitis (Nakarsa) (W=0.787)*** Tick infestation (W=0.397)** Increased cattle movement (W=0.839)***

Wildlife Contact (W=0.287)* 8.5(2-12) 4.5(0-10) 4.5(2-8) 2.5(0-10)

N=10; W, Kendall’s coefficient of concordance (*P <0.05; **P <0.01; ***P< 0.001). The number out side the bracket represents medians and minimum and maximum values are in the bracket. The agreement was termed weak, moderate and good if W-values were less than 0.26, between0.26 and 0.38 (p < 0.05) and greater than 0.38(p< 0.01 to 0.001), respectively (Seigel and Castellan, 1994). From the 116 herds examined for the presence of antibodies to 3ABC non-structural protein of FMD virus, at least one animal tested positive in 64 herds (55.2% of herds) and 21% of individual (n = 920) tested positive. Out of 120 samples randomly selected from 193 positive sera for serotyping using liquid phase blocking ELISA, 99.2%, 95.8%, 80.0%, and 67.5% were positive, respectively for O, A, SAT2 and C serotypes. Of the 50 herds that were sampled, 41 (82 %) of the herders reportedly observed clinical FMD in their herds at various times between Dec. 2004-Nov. 2005. The accuracy of the herder diagnosis was further shown by calculating the positive predictive value (PPV) based on the herd level diagnosis and the 3ABC ELISA test results. Calculations demonstrated that the PPV of herder diagnosis of FMD at herd level is 93.1% (95% CI = 78.0%, 98.1%). This validates the matrix scoring and Proportional piling data on disease characterisation, incidence and mortality. The detection of a non-structural protein, 3ABC is currently regarded as reliable indicator to show FMD virus infection. The antibody to the 3ABC protein persists in affected animals for over one year (up to 395 days) post infection.

4.5(2-7) 3(2-4) 11.5(7-16) 0.5(0-6)

9.5(0-13) 3(0-7) 5(3-9) 2(0-10)

1.5(0-5) 5(3-6) 2(0-6) 11.5(9-14)

4. DISCUSSION

The study showed that Borana pastoralists described clinical and epidemiological features of FMD according to typical descriptions of the disease in veterinary textbooks. Pastoralist perceptions of the clinical signs of acute and chronic FMD (Table 1), age specific incidence and mortality due to FMD (Fig 1) and seasonal variations in FMD outbreaks associated with cattle movement (Table 2) were all consistent with modern veterinary thinking (Radostits et al.1994). The clinical signs of chronic FMD (gaandile) reported by Borana herders were similar to those reported in cattle in pastoralist areas of Afar region (Tadesse, 2003) and Somali region (Eshetu 2003) in Ethiopia, and in Maasai areas of Tanzania (Catley et al. 2004). Up to 12.8% of acute FMD cases in Borana cattle later developed signs of chronic FMD, and this was similar to the 12.0% of Maasai cattle developing chronic FMD after acute disease (Catley et al. 2004). Incidence estimates (Fig 1) and herd seroprevalence estimates (Table 3) indicated that FMD was endemic in Borana pastoral system. FMD was also reported as one of the main diseases of Borana cattle more than 15 years ago (Coppock 1994), indicating the long-term presence of the disease. Compared to other cattle diseases, FMD cases in our study were observed by pastoralists more frequently than any other disease. The overall seroprevalence of 21% (55.2% of Borana herds) was similar to the 26.5% seroprevalence reported elsewhere in Ethiopia (Sahle 2004). Although we did not aim to quantify the risk factors associated with FMD outbreaks, the seasonal calendar (Table 2) suggested a link between FMD outbreaks and cattle movement during the two dry seasons. In Borana production systems, the forra herd comprises the majority of the cattle and these herds are moved during the dry season to access grazing and water. Herds from different areas congregate around these resources as the dry season progresses and theoretically, contact between herds would enable transmission of FMD virus. Research on transhumant Fulani cattle in

The Global control of FMD- Tools, ideas and ideals – Erice, Italy 14-17 October 2008

5. ACKNOWLEDGEMENTS

The authors thank Dr Keith Sumption for his help and FAO EMPRS for the financial support and Dr Andy Catley and Dr Brihnu Admasu for reviewing the manuscript.

6. REFERENCES

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Cameroon showed that important risk factors in FMD transmission included transhumance and mixing of herds at watering points (Bronsvoort et al. 2004). The detection of FMD serotypes O, A, SAT2 and C in Borana cattle agreed with surveys in the Omo National Park and Bale mountain area of Ethiopia (Sahle 2004), and samples collected during FMD outbreaks in dairy farms in and around Addis Ababa (Dejene 2004). Serotypes O, A, and SAT2 were also isolated from cattle by National Veterinary Institute in Ethiopia during outbreak investigations between 1982 and 2000 (Gelaye et al.2001). This study has shown that participatory epidemiology is one of the options that best complement veterinary disease surveillance. In developing countries where disease surveillance and diagnostic services are not smooth, standardized participatory epidemiological tools can produce quantitative as well as qualitative data that can be used to formulate appropriate global FMD control.

The Global control of FMD - Tools, ideas and ideals – Erice, Italy 14-17 October 2008 [18] Tadesse, G. (2003): Participatory studies on Heat intolerance syndromes Associated with FMD in indigenous cattle in Afar pastoral area of Ethiopia. Faculty of veterinary Medicine, Addis Ababa University, Debre Zeit DVM, Thesis. [19] Thomson, G.R. and Bastos, A.D.S. (2005). Foot-and-mouth disease. In: J.A.W. Coetzer and R.C. Tustin (eds), Infectious Diseases of Livestock, (Oxford University Press, New York), 1324–1366 [20] World Organisation for Animal Health (OIE) (2007): Final report of the 17th conference of the OIE Reginal commission for Africa: strategy for strengthening epidemiological surveillance in Africa, Asmera, Eritria, 26 February- 1 March. OIE, Paris, 53-54.

The Global control of FMD- Tools, ideas and ideals – Erice, Italy 14-17 October 2008