Preventive Veterinary Medicine, 1 (1982) 27--36 27

Elsevier Scientific Publishing Uompany, Amsterdam -- Printed in The Netherlands

THE APPLICATION OF TIME SERIES ANALYSIS TO DETERMINE THE

PATTERN OF FOOT-AND-MOUTH DISEASE IN CATTLE IN PARAGUAY

E D U AR DO A L V A R E Z P E R A L T A t, TIM E. CARPENTER 2 and THOMAS B. F A R V E R 2

'Pan American Health Organization, Caracas (Venezuela)
2Department of Epidemiology and Preventive Medicine, School of Veterinary Medicine,
University of California, Davis, CA 95616 (U.S.A.)
(Accepted 3 February 1982)

ABSTRACT

Peralta, E.A., Carpenter, T.E. and Farver, T.B., 1982. The application of time series
analysis to determine the pattern of foot-and-mouth disease in cattle in Paraguay.
Prey. Vet. Med., 1: 27--36.

The temporal distribution of foot-and-mouth disease (FMD) in cattle in Paraguay,

from 1972 to 1979, was examined using time series analysis. This technique was used to
remove data irregularities which may complicate data analysis. The results showed that
one secondary peak and two major cycles occurred during that period. It was determined
that the secondary peak was due to a sporadic outbreak of FMD caused by type C virus.
The two major cycles were predominantly due to type O virus which was found to have a
3 to 4 year frequency. This temporal pattern may aid administrators by elucidating times
when increased control activities should be implemented to counteract the periodic
epidemics. Time series analysis may be used to evaluate the temporal pattern of other
diseases in addition to FMD, and aid in their control programs.

INTRODUCTION

Foot-and-mouth disease (FMD) is known as one of the most contagious

diseases of farm animals (Brooksby, 1967; Hyslop, 1970; CaUis, 1980).
It is caused by a small virus (family Picornaviridae, genus Apthovirus) which
is classified according to antigenic composition into types and subtypes
(Pereira, 1977). At least seven immunologically distinct types and 64 sub-
types have 6een isolated (Hyslop, 1970; Acha and Szyfres, 1977). The
degree of antigenic difference among the types is so great that there have
been records of animals becoming naturally infected with three different
types of FMD virus within 6 months. However, for each type, recovery
results in a strong immunity to reinfection with virus of the homologous
strain. Such immunity persists for several years. Within the types, the sub-
types exhibit varying degrees of cross-protection (Hyslop, 1970).
In South America, FMD has been present since 1870. That year it was
reported in Argentina, Chile, Uruguay and in the state of Rio Grande do Sul,

0167-5877/82/0000--0000/$02.75 © 1982 Elsevier Scientific Publishing Company

28

Brazil. More recently it was reportedly introduced into Bolivia, Paraguay

and Peru; in 1950, in Venezuela and Colombia; and in 1961, in Ecuador.
Types O, A, and C are present in all these countries with the exception of
Colombia, Ecuador and Venezuela which only have O and A (FAO, 1968--
1980; Machado, 1969; Pollard, 1973; Rosenberg and Goic, 1973; Casas,
1978). Between 1958 and 1973, twenty different subtypes were identified
in South America (Alonso et al., 1973).
Before 1960, perhaps with Venezuela as the only exception, the control
effort in South America against FMD was mainly based on the voluntary
action of farmers. During the 1960's the following nations initiated control
programs: Argentina (1961); Brazil (1965); Paraguay (1968); Uruguay
(1968); Chile (1970); Colombia (1972); Ecuador (1972); Peru (1975);
Bolivia (1975) (Rosenberg and Goic, 1973; Casas, 1978). In general, all
these programs are based mainly on compulsory and systematic vaccination
of cattle, control of outbreaks, and imposition of some restrictions on
animal movement. In certain regions of Argentina and Uruguay sheep are
also vaccinated. Inactivated vaccine is used in all these programs and applied
three times per year in cattle over 4 months of age. In Venezuela, attenuated
live virus vaccine is also used and cattle are vaccinated in this case every 6
months (Casas, 1978).
There is a general consensus that these programs have reduced the num-
ber of outbreaks, the attack rates, seriousness of clinical signs, and physical
losses produced by the disease (Casas, 1978). In fact the program officially
eradicated FMD from Chile in 1981. However, until now, lack of reliable
data has made it difficult to accurately measure the pattern and character-
istics of the disease.
It is known that FMD, like other contagious, endemic diseases, shows a
cyclical and seasonal behavior, which is probably related to factors such as
virus mutation, density of susceptibles, infectivity, contact rates, duration
of ~ickness and resistance (Malaga, 1976; Rubenstein, 1977). It has been
suggested that in the case of FMD, seasonal and cyclical variations are not
affected by massive vaccination (Rosenberg and Astudillo, 1976). On the
other hand, Rubenstein (1977) suggests that a cyclical pattern of the vac-
cination frequency based on the behavior of the livestock producers may
explain cycles in disease incidence under voluntary vaccination schemes.
For this reason, in diseases highly responsive to changes in such regional
level of vaccination, it may be necessary to establish a steady high level of
regional vaccination in order to control epidemics.
In South America the most reliable and complete information available
about FMD frequency is related to the number of affected farms at differ-
ent time periods. The condition of "affected farm" is assumed when a
veterinary professional makes the verification by clinical diagnosis, that on
a farm at least one susceptible animal has signs and/or lesions of the disease.
Using this criterion for an affected farm, it is sometimes almost impossible
to make a differential diagnosis between FMD and vesicular stomatitis
 29

(Cottral, 1 9 7 2 ) a n d laboratory diagnosis is recommended. But field samples

are n o t taken in all the cases and, furthermore, only about a half of the
"affected farms" have positive laboratory confirmation.
In Paraguay during the past several years a massive vaccination program
of the cattle population against FMD has been executed and vesicular
stomatitis has never been recorded. There is relatively good information
a b o u t the number of herds affected b y FMD in Paraguay. For these reasons,
Paraguay was chosen as the source of data for this paper.
The objective of this paper is to apply the classical time series method
of analysis to data from Paraguay as a whole in order to evaluate the tem-
poral pattern of FMD. Time series analysis is an approach which may be
used to answer mathematical and statistical questions posed by time cor-
relations introduced by the sampling of adjacent time points.
Time series analysis may provide a basis for removing irregularities in data
to facilitate epidemiologic evaluations, permit project planning and evaluate
current programs. Information learned from this analysis will be used by the
Inter-American Development Bank in its animal health evaluation model.
In addition, it may be useful as a model to those planning FMD or other
animal disease control programs.

MATERIALS AND METHODS

Data utilized in this work were obtained from publications by the Na-
tional Service for Control of FMD (currently SENACSA, previously SENAL-
FA) of Paraguay (SENALFA, 1968--1979; Arteche, 1974) and the Pan
American FMD Center. In all cases, the focus was on the bovine species and
expressions like outbreak, affected herd or afro-ted farm, mean one or more
bovines affected b y FMD in a ranch, farm, l~olding, pasture or any other
premise.

TABLE I

Outbreaks of FMD reported (total number and by virus type when identified) by year in
Paraguay, 1972--1979 (Source: Servicio Naeional de Lucha Contra la Fiebre Aftosa
(SENALFA))

Number of Years
outbreaks
1972 1973 1974 1975 1976 1977 1978 1979 Total

Total 45 49 59 121 101 43 29 206 653

With O 10 4 4 34 29 14 9 65 169
virus A 2 6 3 4 2 2 0 1 20
identi- C 5 3 14 6 1 4 2 11 46
fication
by type total 17 13 21 44 32 20 11 77 235
30

¢n 5 o
RAW DATA A
.......... 12-MONTH MOVINGAVERAGE /~
40 .... TREND '/~l
1-
30
0
o 2O
L~
m I0

z 0
1972 I 1974 ] 1976 u I 1978 I
REPORTING PERIODS (months)
Fig. 1. F M D o u t b r e a k s r e p o r t e d b y m o n t h , t w e l v e - m o n t h m o v i n g average a n d t r e n d .
Paraguay, 1 9 7 2 - - 1 9 7 9 .

From January 1972 to October 1979, a total of 653 outbreaks of FMD

was recorded in Paraguay (Table I and Fig. 1). From this total, FMD virus
typification was done in 235 (36.0%) of the outbreaks. From these typifica-
tions, t y p e O was identified in 169 (71.9%) instances; type A in 20 (8.5%);
and type C in 46 (19.6%). The monthly distribution of the outbreaks is
presented in Table II.
With this information as a basis, the classical time series decomposition
method was used to determine the underlying pattern of FMD and its
seasonal and cyclical components (Wheelwright and Makridakis, 1973;
Lapin, 1978). This m e t h o d was used in an a t t e m p t to identify three separate
parts of the basic underlying pattern: the trend factor, the cyclical factor
and the seasonal factor. The mathematical form used to represent this model
is:

Yt = Tt X Ct X St X It
where, Yt = the original time series data St = the seasonal factor
h = the irregular or randomness factor Tt = the trend factor
Ct = the cyclical factor t = time period.
The procedure employed (Lapin, 1978) to analyze the data is outlined
below using data from Paraguay as an example. The first step in applying
the decomposition technique of time series was to determine the seasonal
factor, St, present. This was done b y applying the ratio-to-moving average
using a 12 month seasonal cycle (Fig. 1). At this step, the original time
series data, Yt, was divided by the seasonal index which removed the season-
al fluctuation and left a deseasonalized value which is a function of Tt, Ct
and/t.
The seeond step was to determine the straight line that represented the
trend, Tt, in the data. An easy method for doing this is to plot a sample of
the moving average values and then, by visual inspection, to fit the straight
line to the data. A second method, which was used in this paper, is to find
a regression equation with time, in months, as the independent variable and
 31

TABLE II

Number of FMD outbreaks reported by month in Paraguay, 1972--1979 (Source: Ser-

vicio Nacional de Lucha Contra la Fiebre Aftosa (SENALFA))

Year Months
J F M A M J J A S O N D Total

1972 3 1 2 3 1 5 1 2 6 17 1 3 45
1973 7 4 10 5 3 3 2 4 1 3 1 6 49
1974 5 5 10 14 2 2 0 2 4 4 5 6 59
1975 7 1 1 3 6 11 14 13 12 26 10 17 121
1976 23 19 13 11 6 11 3 6 3 2 3 1 101
1977 5 6 4 2 4 9 3 2 3 2 2 1 43
1978 6 0 2 1 4 1 1 0 1 4 4 5 29
1979 9 10 6 2 17 41 52 36 24 9a -- -- 206

Total 65 46 48 41 43 83 76 65 54 67 26 39 653
apreliminary data.

t o t a l n u m b e r o f a f f e c t e d herds, b y m o n t h , as the d e p e n d e n t variable. To d o

this regression, U t i l i t y / M i n i t a b s y s t e m (Minitab II) was used ( R y a n et al.,
1 9 7 6 ) . T h e f i t t e d t o t a l n u m b e r o f a f f e c t e d herds f o r each m o n t h was ob-
t a i n e d using t h e c o m p u t e d regression a n d are t h e m o n t h l y t r e n d values
(Fig. 1).
T h e t h i r d step was t o d e t e r m i n e t h e cyclical f a c t o r C t. First each de-
seasonalized value was divided b y the c o r r e s p o n d i n g t r e n d value and ex-
pressed as a p e r c e n t a g e .

Deseasonalized d a t a Tt X Ct X I t
× 100 = × 100 = Ct × It × 100
Trend Tt
T h e n a 6 - m o n t h m o v i n g average was used t o eliminate t h e irregular f a c t o r ,
h , t h e r e b y isolating t h e cyclical c o m p o n e n t Ct.

RESULTS

A p p l i c a t i o n o f t h e time,series m e t h o d t o t h e d a t a f o r P a r a g u a y s h o w e d
the existence o f cyclical a n d seasonal f l u c t u a t i o n s . Also a v e r y slight b u t sig-
nificant (P < 0 . 0 5 ) increase in r e p o r t e d o u t b r e a k s f r o m 1 9 7 2 t o 1 9 7 9 was
observed (Fig. 1).
In Fig. 2, t w o cycles b e t w e e n 1 9 7 2 a n d 1 9 7 9 can be o b s e r v e d : o n e f r o m
1 9 7 2 t o 1 9 7 5 a n d t h e o t h e r f r o m 1 9 7 5 t o 1 9 7 9 . T h e r e is a m i n o r p e a k be-
t w e e n 1 9 7 2 a n d 1 9 7 5 w h i c h is n o t p r e s e n t b e t w e e n 1 9 7 5 a n d 1 9 7 9 .
T h e seasonal e f f e c t is expressed as an i n d e x (Wheelwright a n d Makridakis,
1 9 7 3 ; L a p i n , 1 9 7 8 ) . It s h o w s , f o r each m o n t h , h o w t h a t m o n t h l y value
relates t o t h e a n n u a l value o f t h e F M D o u t b r e a k s . In Fig. 3 a n d Table I I I
it can be seen t h a t J a n u a r y , M a r c h , J u n e a n d O c t o b e r have values higher
t h a n t h e a n n u a l value. Also April, M a y , J u l y , A u g u s t a n d N o v e m b e r are
 ¢.O
bCJ

T A B L E III

Calculation of seasonal i n d e x e s f r o m p e r c e n t a g e s o f m o v i n g average f o r t h e n u m b e r of F M D o u t b r e a k s b y m o n t h s in

Paraguay, 1 9 7 2 - - 1 9 7 9 (Source: Servicio N a c i o n a l de L u c h a C o n t r a la F i e b r e A f t o s a ( S E N A L F A ) )

Year Months
J F M A M J J A S O N D

1972 25.6 47.6 127.7 333.3 18.9 56.6

1973 134.6 75.5 192.3 113.6 78.9 75.0 50.0 100.0 25.0 68.2 21.3 130.4
1974 111.1 116.3 227.3 311.1 41.7 40.8 0.0 40.8 83.3 114.3 151.5 157.9
1975 145.8 17.2 15.2 38.5 66.7 114.6 129.6 106.6 89.6 181.8 68.5 116.4
1976 163.1 141.8 102.4 97.3 60.0 120.9 39.0 93.8 54.5 42.6 69.8 24.4
1977 125.0 157.9 108.1 54.1 111.1 250.0 83.3 58.8 96.8 66.7 69.0 38.5
1978 272.7 0.0 111.1 55.6 200.0 43.5 40.0 0.0 27.0 102.6 88.9 74.6
1979 84.1 68.5 35.3 11.0

M e d i a n (Me) 134.6 75.5 108.1 55.6 72.8 94.8 40.0 58.8 83.3 102.6 69.0 74.6

Seasonal
166.6 93.4 133.8 68.8 90.1 117.3 49.5 72.8 103.1 127.0 85.4 92.3
index

12
Mei = 969.7
i=1
1200 1200
Seasonal i n d e x x Mei - x Mei
Mei 969.7
 33
I--
zw 300-
z
OA

g 200
0 ,,.-
(.91--
-%
< I00
_J
>-
c~ 0
' 1972 ' 1974 I 1976 I 1978 I
REPORTING PERIODS (months)

Fig. 2. Cyclical component of all FMD reported outbreaks in Paraguay, 1 9 7 2 - - 1 9 7 9 .

150
x
~J
c~
Z
I00
d
<
Z
O
tf)
< 50
[aJ
o3

0
I I I I I t I I I INO /V I
JAN MAR MAY JUL SEP
FEB APR JUN AUG OCT DEC

SEASONS(months)

Fig. 3. Seasonal index for the number of FMD reported outbreaks in Paraguay, 1 9 7 2 - -
1979.

clearly below the annual value with the remaining three months close to the
annual value.
Between January 1 9 7 2 and October 1979, FMD virus type O was isolated
and identified from 169 outbreaks, representing 71.9% of the total number
of affected farms in which virus identification was performed (Table I). A
cyclical behavior in the frequency of FMD virus type O was observed when
the classical decomposition time-series method was applied to the monthly
distribution of FMD in which virus O was isolated (Fig. 4).

DISCUSSION

The results of this time-series analysis point to the existence of trend,

seasonal and cyclical components as important aspects of the pattern of
34

300 -

z
w
z
o ~ 200

<

.J ~ I00
o
).-

I19721 I 19741 I 19761 I 1978{ t

REPORTING PERIOD
Fig. 4. Cyclical component of the FMD reported outbreaks in which virus type 0 was
isolated. Paraguay, 1972--1979.

FMD in Paraguay. The trend of FMD from January 1972 to October 1979
shows a slight increase over the period (Fig. 1). The epidemic that occurred
in 1979 can explain the slight increase of the trend line. The implication of
the trend c o m p o n e n t is that the disease will continue to persist if the cir-
cumstances remain the same.
The seasonal c o m p o n e n t analysis shows that in certain m o n t h s the disease
incidence is relatively high compared with other months. The most likely
explanation for these seasonal highs is t h a t they are related to the vaccina-
tion program in Paraguay and changes in the dissemination rate of the FMD
from affected to susceptible herds. The vaccination program can be related
to the seasonal variations because vaccination is performed every year only
during certain months: January, May and September from 1972 to 1975;
January, May and October in 1976; and February, June and October since
1977. This means that the detection of the disease is more likely during
the m o n t h s of vaccination because more personnel are in the field and can
therefore observe the disease, if present. Thus, this factor alone can cause
the number of reported FMD outbreaks to appear to have seasonal varia-
tions.
Also, the animals are assembled at one place in order to administer the
vaccine. In some cases, these are only animals from one farm, but in other
cases, animals from neighboring farms are brought together. Both cases re-
present situations where the dissemination rate can easily increase due to
close contact of animals and therefore increase the number of FMD out-
breaks.
 35

The cyclic behavior of FMD outbreaks was seen to have a frequency of

3--4 years. A common explanation is that there are changes in the composi-
tion of the cattle population such that increasing numbers of susceptible
animals are present periodically (in this case and for the period of the
analysis every 3--4 years) creating situations conducive to epidemic out-
breaks. Some authors (McVicar and Sutmoller, 1976; Rosenberg and Astudil-
lo, 1976)suggest that vaccination programs do not alter seasonal and cyclical
variations, saying that humoral antibodies do not significantly influence
local FMD virus growth in the pharynx of infected animals.
It was found in this analysis that FMD virus type O had a pattern that
fixed the shape of the cyclic behavior of FMD in the eastern region and also
for the country as a whole. The exception for Paraguay as a whole was a
secondary peak in early 1974. The explanation is that in 1974 an epidemic of
FMD virus type C affected especially the Mennonite Colonies of the western
region and this corresponds to the secondary peak seen in Fig. 2 which
shows the cyclic pattern of FMD for Paraguay as a whole. Thus, clearly it
is FMD virus type O that predominantly causes the cyclic behavior of FMD
outbreaks in Paraguay. However, these cycles appear shorter than the 4--5
year cycles mentioned for this type in South America (Rosenberg and
Astudillo, 1976). With this information, disease control program adminis-
trators in FMD type O, endemic countries should reevaluate their programs
particularly focusing their efforts on the predicted periodic epidemics.

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36

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