M. Aminjanov & S. Aminjanov / Echinococcosis and research in Uzbekistan
13
Еchinococcosis and research in Uzbekistan
M. AMINJANOV & S. AMINJANOV
Uzbek Scientific Veterinary Research Institute, 704453 Tailyak Rayon, Samarkand, Uzbekistan
ABSTRACT
Over the past 10 years, the numbers of cases of human echinococcosis in Uzbekistan has increased
by a factor of 3.7 and, in some regions, the annual human incidence is now greater than 10 cases per
100,000 population. In farm livestock and dogs, the prevalence of infection has increased
substantially in the same time period. The prevalence in sheep is now over 62%, that of cattle greater
than 42%, goats 11%, camels 35%, and donkeys 38%. Prevalence rates in dogs are generally about
28% in rural areas. Experimental infections in dogs suggest that the prepatent period of
Echinococcus granulosus
varies with the season of the year: the longest prepatent period (about 90
days) being in the winter, the shortest (about 31 days) being in the summer. We recommend that, in
areas of high livestock infection, dogs should be treated with anthelmintics 8 times per year. We
have tested the efficacy of a number of anthelmintic products to find the cheapest effective
preparation for use in Uzbekistan. We also recommend that all infected stock should be incinerated
when slaughtered to prevent transmission to dogs.
Эхинококкоз и его изучения в Республике Узбекистан
М. АМИНЖАНОВ & Ш. АМИНЖАНОВ
Узбекский научно-исследовательский ветеринарный институт, 704453, Тайляк р-н, Самарканд обл.,
Узбекистан
V
РЮЗЮМЕ
Республика Узбекистана относится к числу эпидемических зон по эхинококкозу. Рост
эхинококкоза за последний 10 лет составляет 3,7 раза.. Пораженность эхинококкозом среди
крупного рогатого скота вырос в два раза, мелкого рогатого скота - в полтора раза, собак -
почти в два раза. Установлена различия в сроках развития эхинококка в кишечнике собак в
зависимости от сезонов года, кормления, содержания и их возраста в пределах одной
республики. Выявлено, что развития эхинококков в кишечнике собак в условиях Республики
летом завершится к 31-му дню, а зимой 83-му дню. С учетом биологии эхинококка
разработана новая технология дегельминтизации собак, состоящая из преимагинальной и
имагинальной. Сочетание этих двух дегельминтизации, проводимые 8 разов в год,
обеспечивают быстрейшего оздоровления хозяйств и населенных пунктов от эхинококкоза.
Разработанная новая технология дегельминтизации собак лечебными гранулами,
содержащих антгельминтики оказался малотоксичной, дешевой и приемлемой во всех
условиях
ведения
животноводства
Республики.
Парэнтеральное
применение
антгельминтиков против эхинококкоза собак обеспечивает полное изгнание гельминтов из
организма собак. Предложенные в практику бетонные резервуары для обеззараживания
пораженных органов эхинококкозом животных и бетонные печи для сжигания бракованных
органов, являются приемлемым и в условиях пустыни, гор и отгонного овцеводства.
14
M. Aminjanov & S. Aminjanov / Echinococcosis and research in Uzbekistan
INTRODUCTION
Echinococcosis is a serious and widespread disease causing serious human health problems and
economic damage to the livestock industries in Uzbekistan. According to data from the Ministry of
Health, during the period 1988-2001,11,239 people were diagnosed with the disease. During the last
10 years the number of people infected has increased by 3.7 times.
Nazirov (2002) reports that between 1999 and 2001, 4,109 people were operated on for
echinococcosis. The analysis of the data shows that echinococcosis is frequently distributed amongst
children and young adults. In 2000, 14.3% of cases were in children less than 14 years of age. Of
the 85.7% adults, 54% were women and 46% men. In 2001, proportion of paediatric cases had risen
to 20.4 % whilst of the adult cases 50.9% were women and 49.2% men. Between 20% and 30% of
cases had recurrences after surgery, whilst surgical case mortality rates were was between 2% and
5%. Boimuratov (1996) analysed 86 paediatric case histories from the children’s surgical hospital in
Sammarkand. Of these cases 27.9% were in children less than 7 years of age, 25.6% in children of
8-10 years and 46.5% in children 11 -15 years of age. The overall incidence rates for human
echinococcosis are highly variable, with very high levels (> 10 cases/100,000) recorded in Bukara
and Sirdarin Oblasts and less than 1 case per 100,000 in Tashkent and Djinzal Oblasts. The regional
incidence of echinococcosis is detailed in Table 1.
Table 1.
The regional incidence (annual cases pre 100,000 population) of Uzbekistan.
Oblast
Incidence (cases per 100,000)
Andijan
2.90
Buhara
11.81
Dj inzak
0.76
Kashkadarini
7.46
Navoin
5.67
Namangent
5.28
Samarkand
3.67
Surhandarin
6.35
Sirdarin
10.16
Tashkent
0.15
Fergan
9.39
Horezm
14.55
Tashkent City
1.68
Uzbekistan
1.53
Paralleling the rise in the incidence of human echinococcosis has been an increase in the prevalence
of echinococcosis in animals. Between 1990 and 2002, the prevalence rate in sheep has increased
from 45% to 62% whilst in cattle it has increased from 24% to 45%.
Data of the prevalence rates in agricultural animals and dogs is presented in Table 2.
Recently we have undertaken a study of the prevalence rates in dogs by purging 531 dogs
with arecoline from 9 different townships. Both village dogs and farm dogs were investigated. The
results are detailed in Table 3.
Prevalence rates varied quite considerably, but farm dogs were significantly more heavily
infected than village dogs overall which is consistent with findings from a similar study in
Kazakhstan (Torgerson
et al
2003). The widespread infection df dogs in Uzbekistan indicates the
low level of anthelmintic prophylaxis used or the poor efficacy of arecoline. Even when
M. Aminjanov & S. Aminjanov / Echinococcosis and research in Uzbekistan
15
successfully purged, an infected dog can still contaminate the environment for 36 hours. New
preparations such as praziquantal, cestel, kanikbantel and others, which have better efficacy than
arecoline, have become available but are too expensive for widespread usage.
Table 2.
Prevalence rates in domestic livestock and dogs between 1990 and 2002.
Prevalence rates
1990
1993
1996
1999
2000
2001
2002
Cattle
24.3
27.6
26.2
31.0
36.3
38.2
45.5
Sheep
45.1
48.3
54.5
57.0
59.1
61.0
62.2
Goats
8.0
8.7
9.3
10.1
9.0
9.5
11.1
Pigs
6.0
6.5
8.0
—
—
—
—
Camels
25.4
28.3
31.0
29.4
31.1
33.0
35.0
Donkeys
32.0
34.3
37.1
36.5
36.4
38.0
38.5
Dogs
15.0
18.4
18.9
20.1
22.5
24.5
28.6
Table 3:
The results of a study where 531 were purged with arecoline from 9 different areas of
Uzbekistan
Study
T
o
ta
l
in
v
e
st
ig
at
ed
N
u
m
b
er
i
n
fe
ct
ed
x©
Farm Dogs
Village dogs
T
o
ta
l
in
v
e
st
ig
at
ed
N
u
m
b
er
i
n
fe
ct
ed
_____
X©
O
4
T
o
ta
l
in
v
e
st
ig
at
ed
N
u
m
b
er
i
n
fe
ct
ed
x© o
4
Mulk
265
35
13.2
134
23
17.1
119
12
10.0
Saxoba-ota
89
15
16.9
15
12
80.0
74
3
4.0
Olga
52
9
17.3
34
7
20.6
18
2
11.0
Upus
15
3
20.0
15
3
20.0
-
-
Kattakurgan
13
2
15.4
13
2
15.4
-
-
Amasai
27
4
14.8
27
4
14.8
-
-
Darvoza
7
1
14.2
7
1
14.2
-
-
Erembe Tova
12
2
16.7
12
2
16.7
-
-
Amangeldi
51
4
7.8
22
2
9.0
29
2
6.8
Total
531
75
14.2
279
56
20.1
240
19
7.9
SEASONAL DEVELOPMENT OF
ECHINOCOCCUS
IN THE DEFINITIVE HOST.
There are a variety of opinions in the literature regarding the development time of
Echinococcus
in
dogs with suggested prepatent periods of between 24 and 90 days. (Sibold 1853, Kuchenmeister
1855, Yamashita
etal
1958, Reddy & Suvamarumari 1971,Bandai 1948, Nosik 1953, Gorina 1962,
Zenkov & Slepnev 1974,
Razakov et al
1986). The variance in the reported development time seems
to depend upon the country in which the studies were undertaken. Reddy & Suvamarumari (1971)
reported in India that the development of the parasite is completed by day 83. However, Pandgy
(1972) asserts that patency begins after 42 days. Zenkov and Slepnev (1973) in Belarus observed,
that full development of the cestode
16
M. Aminjanov & S. Aminjanov / Echinococcosis and research in Uzbekistan
occurs between 43 and 66 days after infection. In our opinion, fluctuation in the development of
Echinococcus
in the intestines of dogs depends on many factors, which have not been studied
sufficiently. These include the age of dogs, how they are maintained, seasonal variations and climatic
conditions. Some of these factors may accelerate development whilst others may slow development
down. Therefore a worming programme may need to be varied between countries or even within one
country depending on these factors. Consequently, we have studied the development of
Echinococcus
in the intestines of dogs in conditions ecountered in Uzbekistan in the winter, summer
and in the autumn.
A total of 12 dogs were each experimentally infected with 25,000 viable protoscolices. The
dogs were all of similar age and breed. There were 3 experimental groups of 4 dogs. One group was
infected in the summer, one in the autumn and one in the winter. Faecal examinations were started
at 25 days of infection and were continued on a daily basis until all dogs in the group had eggs and
proglottids in the faeces. The dogs were then euthanised and the adult parasites were recovered from
the small intestine. The total number of parasites were enumerated, the sizes of the parasites from a
representative sample from each group of dogs was determined and the morphology and sexual
maturity of the proglotids determined. The results are summarised in Table 4.
In the group of 4 dogs infected in the summer, eggs were first detected in the faeces of 1 dog
31 days after infection and by 35 days after infection all animals had patent infections. At necropsy,
on day 35 a total of 78,318 adult parasites were recovered with a mean of 19,579.5 from each dog
(Table 3). The detailed morphology of 535 adult parasites recovered from these dogs was
investigated. Of these, 55.6 % had three proglotids whilst 44.4 % had 4 proglotids. The length of the
strobila ranged from 2.040 up to 3.0 mm, whilst the length of the last proglotid ranged from 0.990
to 1.950 mm. The last proglotid was filled with mature eggs. These data indicate that in the summer
in Uzbekistan
E. granulosus
reaches sexual maturity by 31 days after infection.
In the second experiment of 4 dogs infected in the month of September, eggs were detected
in the faeces at between 39 and 43 days after infection. At post-mortem, 45 days after infection,
47,697 adult
E. granulosus
were found, with an average of 11,924 in each dog. Detailed examination
of 283 parasites demonstrated that 11.2% had 2 proglotids, 66.6% had 3 proglotids and 22.2% had
4 proglotids. The length of the strobila were between 4.02 and 5.394 mm, with the length of the last
proglotid between 2.215 and 3.018 mm. The uterus was filled with mature eggs. This data suggests
that the prepatent period of
E. granulosus
is 39 days in the autumn.
In the dogs infected in the winter, the first eggs and proglotids were observed in the faeces
on the 83
rd
day after infection. The dogs were necropsied at 97 days after infection when all dogs
had patent infections. A total of 41,638 parasites were recovered with an average of 10,409 in each
dog. Of 256 parasites examined in detail, 91.6 % had three and 8.4 % had four proglotids. The lengths
of the strobila were between 3.534 and 4.253 mm, and the length of the last, mature proglotid was
1.612-2.046 mm. The last proglotid was filled with mature eggs.
These experiments suggest that the prepatent period can vary considerably between
summer and winter. In winter, it is 52 and 44 days longer than in summer and autumn respectively.
Therefore, the period between anthelmintic treatment can be varied accordingly. This data also
suggests that the size of the mature parasites vary according to season, being largest in autumn and
winter and smallest in summer.
M. Aminjanov & S. Aminjanov / Echinococcosis and research in Uzbekistan
17
Table 4.
Development of
Echinococcus granulosus
in the intestines of a dog during different
seasons of the the year. Each dog was experimentally infected with 25,000 viable protoscolices.
N
o
o
f
D
o
g
D
at
e
o
f
in
fe
ct
io
n
T
im
e
o
f
o
cc
u
rr
en
ce
o
f
eg
g
s
an
d
p
ro
g
lo
ti
d
s
in
t
h
e
fa
ec
es
af
te
r
in
fe
ct
io
n
.
T
im
e
o
f
n
ec
ro
p
sy
o
f
d
o
g
af
te
r
in
fe
ct
io
n
N
u
m
b
er
of
E
ch
in
o
co
cc
u
s
f
o
u
n
d
Me
an
s
tr
o
b
il
a
le
n
g
th
(
m
m
)
Me
an
l
en
g
th
o
f
la
st
p
ro
g
lo
ti
d
(
m
m
)
Mo
rp
h
o
lo
g
y
o
f
u
te
ru
s
in
la
st
s
eg
m
en
t
Summer
1
2
3 ■
4
Mean
10.07
10.07
10.07
10.07
33
31
32
35
35
35
35
35
21978
18317
19532
18491
19579.5
2.045
2.538
2.126
3.000
2.427
0.970
1.410
1.105
1.830
1.329
Filled with mature eggs
Autumn
5
6 7 8
Mean
20.09
20.09
20.09
20.09
44
41
39
43
45
45
45
45
11910
13427
10925
11435
11924.2
4.050
4.895
5.394
5.203
4.885
2.110
2.950
3.018
2.946
2.756
Filled with mature eggs
Winter
9
10
11
12
Mean
5.12
5.12
5.12
5.12
88
83
86
91
97
97
97
97
9356
1087 11547
9864
10409.5
4.253
4.036
3.534
3.820
3.911
2.046
2.018
1.696
2.010
1.943
Filled with mature eggs
CONTROL OF ECHINOCOCCOSIS
Prophylactic deworming of dogs is important for the protection of the health of people and
agricultural animals. The aim of prophylactic therapy is to ensure dogs are treated before the
infection becomes patent and thus minimise the potential for transmission. In areas where there are
high levels of infection in animals, we believe it is necessary to treat farms dogs with anthelmintics
8 times per year. Of particular importance are treatments in late winter in February or early March;
treatments in late April or early May; treatments in mid summer in June-July; and a fourth treatment
when animals ar$ collected in the autumn.
To undertake the prophylactic treatment of dogs, a platform of 10x20m is necessary, where
it is dry and there is no vegetation, preferably on a concrete surface. Treatment using
18
M. Aminjanov & S. Aminjanov / Echinococcosis and research in Uzbekistan
such a place can be undertaken on 10 dogs at a time. The anthelmintic arecoline is administered
orally, and the process is considered complete when the dogs have defecated 3 times. All faeces and
intestinal materials, together with any cestodes that have been passed are collected and burnt. The
platform is disinfected with 10% chlorite solution. Used gowns, gloves and instruments are
disinfected by boiling. Dogs that have been treated are recorded with their owners’ names. This
should be done 4 times per year. After each prophylactic treatment, owners are given anthelmintics
to administer 30-40 days later. This treatment should not be hazardous as any parasites the dogs may
have will be in the prepaptent period. Thus, this treatment administered by owners is also given 4
times per year. This scheme of anthelmintic treatment should be undertaken where there are the most
intensive populations of dogs. We have also developed a two-stage process for the use of arecoline.
A dose of 5mg/kg of arecoline is administered orally in a 0.1% solution. Any dogs that are seen to
be infected with cestodes at the subsequent purge are given a second treatment. Using this method,
we believe we can eliminate 100% of mature parasite infections and approximately 96% of immature
parasites.
A modem method of administration of anthelmintics is the use of medicated feed for dogs.
A maximum concentration of 10% anthelmintic is given in a product containing 70% wheat flour,
10% sugar, 8% milk, and 2% water. All components are carefully mixed and made into a bait, dried
and stored in the dark for up to 1 year.
It is important that anthelmintic preparations are cheap and effective. Bunamidine
hydrochloride at a dose of25-50 mg /kg is reported to be 100% effective against
E. granulosus
90
days after infection. In a trial involving 25 dogs we found that parasites were completely eliminated
in 24 dogs after 2 doses of bunamidine, and the overall parasite burden was reduced by 99%. We
have also found that bunamidine has a good prophylactic effect when mixed with food granules and
at doses of up to 120 mg/kg does not appear to have side effects in dogs.
Geksohlorofen at a rate of 15mg/kg has an efficacy of 78.5% against immature
E.
granulosus,
rising to 100% with a second dose. At 50mg/kg the efficacy rises to 100% against both
mature and immature parasites. The preparation cetovex (Rhone-Poulonc) has good prophylactic
effect with a dose rate of 25 mg/kg being 97.4-99.4 % effective. We have also investigated the
efficacy of praziquantal as an injection, tablet and in medicated granules. We have found that at the
dose of 2.5-5.0 mg/kg the preparation is 100% effective against juvenile and adult stages of
E.
granulosus
in dogs. We have also developed a new anthelmintic based on copper salts (cestan) in a
fodder granule formulation, which is effective against the immature and mature forms of
E.
granulosus
at 150mg/kg. The development of this product in particular means that we can avoid the
importation of expensive and potentially toxic preparations from foreign countries.
One problem with the oral administration of anthelmintics is the possibility that the
preparation is degraded by the acidic conditions in the stomach before it reaches the small intestine.
Because of this we have developed an injectable anthelmintic preparation. This consists of 5%
febantal, 10% fenasala and 3% mebendazole. This preparation at a dose of 25-50mg/kg given
intramuscularly 25 days after experimental infection has an efficacy of between 74.4 % and 100.0
%. Mebendazole on its own appears to be 100% effective when given as a 3% injectable solution at
a dose of 50.0 mg/kg.
'
A very important aspect of the control of echinococcosis is the proper disposal of corpses of
agricultural animals. We recommend that such animals are placed in secure
M. Aminjanov & S. Aminjanov / Echinococcosis and research in Uzbekistan
19
concrete tanks and incinerated wherever possible. Alternatively corpses treated with 10%/ formulin
or 7% chlorite render cysts non infectious to dogs after 7-10 days.
J
REFERENCES
В
AD ANIN N.B. (1948) Questions about the epizootiology of
Echinococcus. Tr UZGSH
5,
111-113
BOYMURATOV N.S. (1996) The surgical treatment of hepatic echinococcosis in children (clinical and
experimental studies). Abstract of the Dissertation for the Master of Medical Sciences. Tashkent, 20 pp.
GORINA N.S. (1962) About the susceptibility of various kinds of carnivores to infection with alveolar
echinococcosis.
Transactions of a Scientific Conference
VOG 1, 43-45
KUCHENMEISTER G.T. (1855) Die in und an dem Korper des Lebenden Menschen vorkommende parasiten.
Avt. die Tierische Parasiten. Leipsig, p481.
NAZIROV F. (2002) Echinococcosis in Uzbekistan: types of problems and methods to improve treatment.
Medical Journal of Uzbekistan
2-3,
2-5.
NOSIK A.F. (1953) Echinococcosis of animals and control measures. Dissertation for the Candidate of
Veterinary Science.
PANDEY V.S. (1972) Observation on echinococcosis in Bihar.
Indian Journal of Animal Science
41,
596-599.
RAZAKOV S (1986) Features of the epizootiology and epidemiology of echinococcosis in Samakand Oblast.
Proceedings of the Scientific Work “Medical Parasitic Problems of Uzbekistan” pp 36- 43.
REDDY CRRM & SUVARNARUMARI G (1971) Biology of
Echinococcus granulosus
as it occurs in south
India.
Acta Tropica
28,
311-322.
SIBOLD C.T. (1853) Uber die Verwandlungder
Echinococcus
Bruten Taenien. Zeitschr. F. Wissensch, IV.
Leipsig, pp 409-425.
TORGERSON P.R., SHAIKENOV B.S., RYSMUKHAMBETOVA A.T., ABDYBEKOVA A.M.,
USENBAYEV A.E. & BAITURSINOV K.K. (2003) Modelling the transmission dynamics of
Echinococcus granulosus
in dogs in rural Kazakhstan.
Parasitology
126,
417-424.
YAMASHITA I. (1958) Studies on
Echinococcus
Differences in development of the tapeworm stages between
E.granulosus
and
E.multilocularis. Japanese Veterinary Journal
6,
226-229.
ZENKOV A.V. & SLEPNEV N.K. (1974) About the maturation of
Echinococcus granulosus
in the dog.
Works
of the Belarus Scientific Veterinary Institute
1,
97-99.
