CHAPTER TWENTY

Seroprevalence and incidence

of human toxocarosis in Russia
Lyudmila V. Akhmadishinaa, Maria N. Ruzinaa, Maria A. Lukashevaa,
Karen K. Kyuregyanb,c, Mikhail I. Mikhailovb,c,
Alexander N. Lukasheva,*
a
Martsinovsky Institute of Medical Parasitology, Tropical and Vector-Borne Diseases, Sechenov University,
Moscow, Russia
b
Russian Medical Academy of Continuous Professional Education, Moscow, Russia
c
Mechnikov Research Institute for Vaccines and Sera, Moscow, Russia
*Corresponding author: e-mail address: alexander_lukashev@hotmail.com

Contents
1. Toxocariasis incidence in Russia 420
2. Toxocariasis seroprevalence in Russia 421
3. Assay sensitivity 427
4. Assay specificity 428
5. Conclusion 429
Acknowledgements 430
References 430
Further reading 432

Abstract
Overall incidence of toxocariasis in Russia is low and varies between 1.6 and 2.7 per
100,000, while in several hyper-endemic regions, such as Altay, Kurgan, Perm and
Udmurtia, it reaches 43 per 100,000. The seroprevalence of toxocariasis in published ref-
erences was on average 16% and varied across the regions of Russia from negligible in
North Siberia to 40% in southern regions of West Siberia. Seroprevalence in adults in
five regions of Russia identified in this study was on average 20%, and varied from
3% in Yakutia (north of East Siberia) to 36% in Rostov-on-Don, South Russia. There
was no correlation between seroprevalence and reported incidence of toxocariasis;
however, the pattern of seroprevalence variation could be linked to Toxocara preva-
lence in dogs. Toxocariasis seroprevalence has more than doubled over the last 20 years.
Diagnostic antibody titres (1:800 or more) were found in 3.6% of sera, suggesting about
five million of acute Toxocara invasions per year.

Advances in Parasitology, Volume 109 # 2020 Elsevier Ltd 419

ISSN 0065-308X All rights reserved.
https://doi.org/10.1016/bs.apar.2020.01.015
420 Lyudmila V. Akhmadishina et al.

1. Toxocariasis incidence in Russia

The registered incidence of parasite infections in Russia has been
decreasing over the last few decades, but they remain a significant socio-
economic burden and a permanent healthcare concern. All parasitic infec-
tions are notifiable, and confirmed human cases have to be submitted to
the reporting system and are included within regular incidence reports
issued for most of the 85 administrative territories, as well as for the country
as a whole; however, the diagnostics quality and the stringency of report-
ing may vary between diseases and administrative regions. The most com-
mon human parasite infections are enterobiasis (215,000 240,000 cases
per year), ascaridosis (22,000–40,000 cases per year), and opisthorchiasis
(20,000–33,000 cases per year) (Rosstat, 2017). Most of these cases are found
upon systematic screening, which is mandatory for admission to public kin-
dergartens, schools, swimming pools, permission to work in healthcare,
education, food manufacturing, and sales. The screening is done by micros-
copy of faeces and anal smear/print for enterobiasis screening. As human
toxocariasis does not result in the shedding of helminth eggs, it is not
detected by this systematic surveillance, and only overt cases, proven by
the detection of high anti-Toxocara IgG levels, are registered. Despite this
serious limitation, there are around 2000 cases of toxocariasis per year in
Russia, or 1.6–2.7 per 100,000 of the population (Yerofeeva, 2017). The
registered incidence of toxocariasis was very low in the 1990s, likely due to
low awareness and poor diagnostics; the incidence increased several times
upon the wide-spread introduction of ELISA, peaking in 2007, and has been
slightly decreasing over the last decade (Fig. 1). The incidence is 2–3 times
higher than the average in children below 17 years of age, and the highest
(about 4–5 times higher than the average, 10–11 per 100,000) in children
aged 3–6 years old (Stepanova and Kornachyov, 2013; Yerofeeva, 2017).
The highest incidence of human toxocariasis is registered in West Siberia
and the Urals region, followed by Central Russia (Volga region) and the
Far East. The incidence in the Altai region (South of West Siberia) is the
highest, 43.2 per 100,000, about 20 times higher than the country average,
followed by Kurgan, Perm, and Udmurtia (Malkhazova, 2015; Starostina
et al., 2015b). A lower incidence is reported in Central and South Russia,
even in areas with an extremely high prevalence (up to 100%) of the parasite
in dogs and in the environment (Akimova, 2006). The reported regional
incidence is patchy, and highly endemic regions may surround regions
Seroprevalence and incidence of human toxocarosis in Russia 421

Incidence of toxocariasis in Russia

Incidence, per 100,000

2

Fig. 1 Incidence of toxocariasis in Russia in 1999–2015 (Guzeeva, 2009; Starostina et al.,

2015a; Yerofeeva, 2017).

with more than a ten-fold lower incidence, or vice versa (Malkhazova,

2015; Starostina et al., 2015b). This suggests that the reporting is non-
uniform, and the published incidence may reflect the awareness of doctors,
the availability of modern diagnostics, and the stringency of the reporting
rather than the true incidence. Also, the stringent case definition and labo-
rious reporting (which is rather avoided than overdone by primary care
personnel) stress that the higher incidence values are more trustworthy
than the lower values.

2. Toxocariasis seroprevalence in Russia

There have been a significant number of toxocariasis seroprevalence
studies in Russia beginning from 1990s (Table 1, Fig. 2). Unfortunately,
a lack of common guidelines and reference panels seriously complicates
comparing the results. This is partially alleviated by the domination of a
single ELISA kit on the market in Russia (also used in this study), but even
then most studies use a titre cut-off of 1:100, while some may set more
stringent titre cut-offs and often do not specify which diagnostic kit was
used and which titre was considered positive; so the results of different
studies are not directly comparable.
The fraction of the seropositive population in various regions of Russia
found in different studies varied between zero and 54% (Table 1). Average
seroprevalence among all published reports was 16%. Values below 5% were
typically reported before 1990. Values above 20% were found in publi-
cations after 2009. This trend was vividly demonstrated in a longitudinal
422 Lyudmila V. Akhmadishina et al.

Table 1 Seroprevalence of Toxocara in Russia.

Region and Seroprevalence,
designation on Fig. 2 Population group % References
Moscow, 1978 (1) All age groups 5.4 Yampolskaya and
Ignashenkova (1978)
Moscow, 1998 (1) Adults 21.3 Guzeeva (2009)
Children 23.5
Moscow, Adults, 50–59 year 29.4 Guzeeva (2009)
2003–2007 (1)
Children, 7–14 year 23.5
Children, 4–6 year 11.8
Moscow region, Adults 30–60 year 24 This study
2008 (1)
Bryansk, Central Adults 3.5 Avdyukhina (1987)
Russia, 1983 (2)
Children <14 year 5.4
St. Petersburgh (3) Children 4.5 Lebedeva (2006)
Rostov, South Adults 22.9 Shishkanova (2011)
Russia (4)
Rostov, South Adults 30–60 year 36.0 This study
Russia, 2008 (4)
Ekaterinburg, South Adults 30–60 year 13.0 This study
Urals, 2008 (5)
Omsk, south of Children <5 year 12.1 Starostina and
West Siberia, Romanova (2016)
2006–2008 (6)
Omsk, south of Children <5 year 32.1 Starostina and
West Siberia, Romanova (2016)
2013–2015 (6)
Omsk, south of Adults 16–60 year 54.1 Berezina et al. (2011)
West Siberia (6)
Children <15 year 40.4
Novosibirsk, south Healthy donors 8.3 Frolova et al. (1997)
of West Siberia,
1997 (7)
Altay, south of West Endemic districts 15.4–40.6 Pautova et al. (2012)
Siberia, <2012 (8)
Non-endemic 2.0–6.0
districts
Seroprevalence and incidence of human toxocarosis in Russia 423

Table 1 Seroprevalence of Toxocara in Russia—cont’d

Region and Seroprevalence,
designation on Fig. 2 Population group % References
Irkutsk, south of Healthy donors 2.4 Kupriyanova (1988)
East Siberia,
Healthy adults 4.7
1977–1987 (9)
Yakutia, north-east Adults 2.6 Avdiukhina and
Siberia, <1994 (10) Lysenko (1994)
Children 0
Yakutia, north-east Adults 30–60 year 3.0 This study
Siberia, 2008 (10)
Khabarovsk, Far Adults 30–60 year 24.0 This study
East, 2008 (11)
Khabarovsk, Far All age groups 15.6 Kozyreva (1999)
East, 1999 (11)

Fig. 2 Map of Toxocara seroprevalence study sites in previous publications (circles) and
€ppen climate
in this study (squares). Numbers correspond to Table 1. Colour indicates Ko
zones according to the legend. The original image was taken from https://en.wikipedia.
org/wiki/Climate_of_Russia.
424 Lyudmila V. Akhmadishina et al.

study of seroprevalence in Omsk in 1995–2010 (Berezina et al., 2011). That

study showed that seroprevalence stayed at around 8% in 1995–2004 and
abruptly increased to 18% in 2005 and over 30% in 2006–2008. Another
study from Omsk reported that seroprevalence almost tripled between sam-
ples collected in 2006–2008 and 2010–2015 (Starostina and Romanova,
2016). It remains unclear if this was an objective increase of seroprevalence,
or a hypothetical change in assay sensitivity. Indeed, all studies in Russia use
an ELISA kit from a sole manufacturer (see below), and simultaneous rapid
increase of seroprevalence in distant areas and in different age groups may
be questionable.
There have been no systematic national/multi-region studies in Russia
similar to those done in other countries (Poeppl et al., 2013; Won et al.,
2008). Moreover, many studies (not discussed in this review) included only
risk groups (children, asthma patients, etc.) and are not representative of the
general population. To provide a reliable image of toxocariasis seropre-
valence in Russia, randomly sampled adult sera from five distant regions
of Russia were investigated using a consistent methodology to provide a
representative image of toxocariasis seroprevalence.
Serum samples were collected from 2007 to 2008 as a part of a hepatitis
B seroprevalence study (Klushkina et al., 2016). Adults aged 30–60 years old
were chosen as a target group. The study subjects were randomly selected
from an address book, and informed consent was obtained. Anonymous sam-
ples were used for this study. Anti-Toxocara antibodies were determined
using the Toxocara IgG ELISA kit (Vector-Best, Russia). According to
the manufacturer’s instructions and state guidelines (2001), antibody titres
equal to or above 1:800 (i.e., that give a positive ELISA signal in dilutions
of 1:800 or above) are suggested as confirmatory for acute toxocariasis, while
titres between 1:100–1:400 may be considered confirmatory in the presence
of compatible symptoms. For this seroepidemiological study, a titre of 1:100
was chosen as positive (as was also done in most previously published
studies), and the positive sera were further titred to a dilution of 1:800,
which was used as a secondary cut-off.
Serum samples were collected in five regions (Fig. 2) representing
Central Russia (Moscow region), South Russia (Rostov-on-Don), South
Urals (Ekaterinburg), East Siberia (Yakutia) and Far East (Khabarovsk).
The seropositivity rates varied from 3% to 36% (Fig. 3). Significantly lower
seropositivity (3%) was observed in Yakutia, while in Rostov-on-Don it
was higher than in other regions (36%). There was no correlation between
seroprevalence and the reported toxocariasis incidence in the study regions
Seroprevalence and incidence of human toxocarosis in Russia 425

Seroprevalence and incidence of toxocariosis in Russia

40
8

Incidence, per 100,000

Seroprevalence, %

30
6

20
4

10 2

0 0
Moscow
region
>1:800 1:100-1:400 Incidence
Fig. 3 Seroprevalence and incidence of toxocariasis in five regions of Russia.

(Fig. 3). The Moscow region featured a high seroprevalence (24%), while
the incidence was 0.03 per 100,000, almost the lowest in the country. Given
the relatively high healthcare level, toxocariasis awareness, and the availabil-
ity of diagnostics in Moscow, the incidence of overt disease in this case is less
likely to be significantly underestimated. On the contrary, the incidence in
Ekaterinburg is among the highest in Russia, about four times the country’s
average, while the seroprevalence (13%) was below average.
The overall fraction of sera with high antibody titres ( 1:800) was 3.6%.
This titre is recommended as a threshold for acute toxocariasis diagnostics.
The fraction of high-titre sera among all positive ones varied from zero to
30%. Similar to general seroprevalence, there was no correlation between
high-titre seroprevalence and incidence. The high-titre seroprevalence var-
ied from zero in Ekaterinburg (high registered incidence) to 11% in Rostov
(low incidence). In the latter case, an incidence of 1/100,000 was accom-
panied by 11% high-titre seroprevalence. Therefore, the registered and
projected incidence differed about 10,000-fold.
A lack of correlation between incidence and seroprevalence has been
also reported in a study done in a hyper-endemic region (Altay, south
of West Siberia). While the incidence ranged between 0.7 and 5.1 per
100,000 in the central districts and reached 77.6 in the Northern region,
the seroprevalence was 10–20% in moderately endemic districts and 17%
in the hyper-endemic ones (Pautova et al., 2012).
Absence of correlation between seroprevalence and incidence can have
several explanations. First, it might be due to an absence of typical clinical
426 Lyudmila V. Akhmadishina et al.

signs, limited diagnostic capacity and a vague case definition. Second, aware-
ness of medical personnel can have an effect, both negative (lack of knowl-
edge) and positive (over-diagnostics). Antigenic cross-reactivity could also
play a role. It is conceivable that all these factors play a role in Russia.
However, the gap between seroprevalence and incidence is huge, especially
in Moscow. Also, the ratio of high-titre and low-titre sera identified in a
single experiment varies across regions.
A lack of correlation between the incidence and the seroprevalence
could be also explained by distinct invasion sources or transmission mech-
anisms. Toxocara eggs were found in 4–10% of vegetables and greenery sam-
ples in Russia (Sabirova et al., 2012; Suleymanova, 2012). This could lead to
common, but low-multiplicity invasion due to a lower number of eggs
in these sources, on average 13.8 eggs per kilogram (Bittirov et al., 2018),
and explain the significant seroprevalence in the absence of overt disease
(as observed in Moscow and Rostov-on-Don) and a low prevalence of
infection in pet dogs in the area (Moscow). This hypothetical food-borne
route could also explain a high seroprevalence in an area with the highest
socioeconomic level (Moscow) because it contradicts the published reports
of significantly higher seroprevalence in risk groups or a socially vulnerable
population (Alvarado-Esquivel, 2013; Antolova et al., 2015). Higher con-
sumption of vegetables and greenery in this economically privileged region
could promote common low-grade invasion. On the contrary, in high-
incidence regions, the classical infection directly from contaminated soil
may be relatively more common, hypothetically more likely to provide
a high infecting dose, and thus a symptomatic disease. Obviously, there
is no direct proof for this hypothesis, and further studies are required to test
the potential impact of distinct infection routes in Russia.
Although there was no systematic data on Toxocara prevalence in primary
hosts in all the study regions, it is worth noting that a high seroprevalence
was observed in the Moscow region. The previously reported seropreva-
lence in Moscow was similar to other regions of Russia, but not lower
(Avdiukhina and Lysenko, 1994; Guzeeva, 2009). At the same time, the
reported incidence of human toxocariasis in Moscow is one of the lowest
in Russia and varies between 0.1 and 0.5 per 100,000. This corresponds
to a low prevalence of infection in pet dogs, below 5% compared to the
30% average in Russia (Lukashev et al., 2020). In this case, the seropreva-
lence was not correlated to the hypothetical low exposure risk from infec-
ted dogs. This observation further stresses that in the case of toxocariasis,
seroprevalence may poorly reflect the overt disease incidence.
Seroprevalence and incidence of human toxocarosis in Russia 427

Significantly lower seroprevalence was found in Yakutia, which has a

cold continental climate with a mean annual temperature of 8.8 °C in
the capital (Yakutsk). The mean daytime temperatures go above 20 °C
in summer, so the development of Toxocara eggs is theoretically possible
(Turbabina et al., 2019), but the permissive season is very short, which
may explain low seroprevalence compared to other regions of Russia.
Unfortunately, there is no data on the prevalence of Toxocara infection
in dogs in Yakutia, so it is not clear if human infections result from a local
circulation, are imported cases, or come from contaminated greenery and
vegetables imported from other regions. The latter supposition is favoured
by the absence of Toxocara seroprevalence in children in Yakutia and low
seroprevalence in adults (2.6%) in 1980s (Avdiukhina and Lysenko, 1994).
Toxocariasis seroprevalence in Russia reported in recent studies (about
20%) was higher than in the United States (5.1% (Berrett et al., 2017) or
13.9% (Won et al., 2008)), the Netherlands (10.7–8.0% (Mughini-Gras
et al., 2016)), Austria (6.3% (Poeppl et al., 2013)). Among European coun-
tries, a comparable seroprevalence (23.5%) was reported in Serbia (Gabrielli
et al., 2017). Higher seroprevalence is typical to Asia, for example, 45.2% in
Vietnam (Nguyen et al., 2016) and Africa, 57.6% in children in Nigeria
(Sowemimo et al., 2017). Seroprevalence in some regions of Russia is very
high even compared to many developing countries and generally corre-
sponds to similarly high prevalence of infection in the main hosts.

3. Assay sensitivity
Although dozens of toxocariasis seroepidemiology studies have been
published in the world, the data is far from comprehensive, largely due to the
limited compatibility of methodology, including sampling and testing
approaches. Moreover, some of the popular testing methods may lack both
sensitivity and specificity to the degree that would seriously complicate the
interpretation of the results (Ma et al., 2018). As antibody titres decrease over
time, this may lead to the under-estimation of seroprevalence. This is
highlighted by the reports of a seasonal pattern of toxocariasis seroprevalence
in Moscow, with the highest values (32–42%) observed in summer and
autumn, and the lowest (11–16%) in winter and spring (Guzeeva, 2009).
A similar seasonal variation of seroprevalence was observed in Omsk
(Berezina et al., 2011). This profile corresponds to seasonal fluctuations in
egg shedding by dogs and the contamination of the environment commonly
observed in Russia (Lukashev et al., 2020), and suggests that at least some of
428 Lyudmila V. Akhmadishina et al.

the seroprevalence studies might predominantly detect recent cases of (re)

invasion. Another study reported the absence of a clear cut-off between
the titres in the “positive” and “negative” sera (Slobodeniuk et al., 2005),
further stressing that the detection of anti-Toxocara IgG does not reflect
lifetime exposure, but a more or less recent infection.
The concern of low sensitivity of the commonly used ELISA tests is also
highlighted by a lower seroprevalence in adults than in children, which was
reported in several independent studies (Avdiukhina and Lysenko, 1994;
Starostina et al., 2015b). It has also been indicated that a positive ELISA sta-
tus persists for just a few years after infection (Deplazes et al., 2011).
However, in studies done in other countries (Berrett et al., 2017) and some
other Russian studies (Avdiukhina and Lysenko, 1994), the seroprevalence
increased over age. Unfortunately, this observation does not necessarily
indicate that seroprevalence corresponds to cumulative exposure because
its increase could have also been attributed to re-infections rather than
persisting antibodies (Deplazes et al., 2011). Therefore, it is not clear to what
extent toxocariasis seroprevalence studies (especially those done with a
stringent titre cut-off ) reflect a cumulative life-long exposure (as they do
for most other diseases), and the data should be treated as the lower estimate
of real toxocariasis exposure.

4. Assay specificity
Specificity is commonly a key limitation of serological tests in hel-
minthology, and in toxocariasis in particular (Ma et al., 2018). Moreover,
it may be difficult to distinguish the effect of cross-reactivity from the input
of risky behaviour and poor sanitary habits that increase chances of infection
with different parasites. In Novosibirsk (Siberia, endemic for Opisthorchis),
8.3% of adults had antibodies to Toxocara, 7.9% to Opisthorchis and 4.6%
to both parasites (Frolova et al., 1997). In Khabarovsk (Far East, endemic
for Clonorchis) 16.4% adults were positive for Toxocara, 14.8% to
Clonorchis and 8.6% to both (Kozyreva, 1999). In both studies the fraction
of Toxocara-positive adults was significantly higher among fluke-seropositive
than among fluke-seronegative individuals. Flukes are not universally pre-
valent in Russia and could not affect the results for all regions. Cross-
reactivity with Ascaris has been the major concern due to phylogenetic
relatedness of the two helminths, relatively high incidence of ascaridosis
in Russia, and published reports of cross-reactivity between Toxocara
and Ascaris suum (Munoz-Guzman et al., 2010). To test cross-reactivity
Seroprevalence and incidence of human toxocarosis in Russia 429

Table 2 Detection of anti-Ascaris IgG in Toxocara-positive sera.

Toxocara IgG Number of Percent of Geometric mean
titre Ascaris-positive sera Ascaris-positive sera of anti-Ascaris IgG
1:100–1:200 5/30 17 1:114
1:400–1:800 11/16 69 1:146
Negative 0/30 0 –

between Toxocara and Ascaris, a panel of randomly selected Toxocara-

positive and negative sera was tested for presence of antibodies to Ascaris
using Ascaris-IgG-ELISA-Best kit (Vector-Best, Russia). An obvious cross-
reactivity was observed. All 30 Toxocara-negative sera were also negative
for Ascaris (Table 2). 16% of sera with a low titre and 67% of sera with
a high titre to Toxocara were also positive to Ascaris. The antibody titres
to Ascaris were almost always lower than to Toxocara in double-positive
sera, and most of the low-titre Toxocara-positive sera were negative for
Ascaris. Therefore, it is unlikely that this cross-reactivity has significantly
affected the Toxocara seroprevalence values, and is rather a concern for
the immunodiagnostics of ascaridosis.

5. Conclusion
The results of this and many other studies show that human infection
by Toxocara is ubiquitous in the human population. The average seroprev-
alence in adults in Russia was 20%. Based upon a suggestion of rapid anti-
body clearance in humans (Deplazes et al., 2011), this corresponds to
roughly 10 million invasions per year in Russia. A comparable estimate
of five million cases can be obtained by extrapolating a ratio of diagnostically
relevant high-titre sera (3,6%) on the population of Russia. The reported
incidence of toxocariasis (about 2000 cases per year) suggests that signifi-
cantly less than 1% of infections are diagnosed. The seroprevalence in
Russia was roughly double that of Europe and the USA, which corresponds
to double the prevalence of Toxocara in its primary hosts. However, there
was no correlation between the seroprevalence of Toxocara in humans
and the prevalence in dogs among the regions of Russia.
A lack of correlation between the seroprevalence and incidence suggests
that the exposure and egg ingestion are necessary, but not the key factors for
the development of the symptomatic human disease. The multiplicity of
infection (amount of ingested eggs) may be a critical factor. Immune status,
430 Lyudmila V. Akhmadishina et al.

healthcare awareness, and the availability of diagnostics are among other

potential explanations.
General improvement of sanitation led to elimination of severe enteric
infections, such as cholera and dysentery, in most countries, but apparently
did not affect toxocarosis. While the increasing seroprevalence found here
may be an artefact, there has been definitely no improvement of the epi-
demiological situation over the last 30–40 years. It is conceivable that a
decreasing awareness to acute enteric infections may even promote an
increasing incidence of toxocarosis. So far, toxocariasis remains ubiquitous,
yet a neglected disease with poorly understood epidemiology, pathogenesis,
and its medical relevance may go beyond our current understanding.

Acknowledgements
This work was supported by the Russian Academic Excellence Project 5-100.

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Further reading
MOSCOW: Ministry of Health of Russia, 2001. Toxocarosis Prophylaxis: Methodical
Guidelines MU 3.2.1043-01. Ministry of Health.