Threats of Vector-Borne Zoonotic Disease in Europe: Dogs, Drosophilids, and Oriental Eye Worm

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the real overall incidence of parasitic diseases declined disease control strategies. China’s experience can be
constantly.7 Under the leadership of the national and shared with the rest of the world.
local governments and implementation of a one-health
strategy, along with close joint multisectoral collaboration Zhongjie Li, *George F Gao
between the departments of health, agriculture, and Key Laboratory of Surveillance and Early-Warning on Infectious
Disease, Chinese Center for Disease Control and Prevention,
the environment, some parasitic diseases have reached
Beijing, China (ZL, GFG); and CAS Key Laboratory of Pathogenic
or approached elimination status. The elimination of Microbiology and Immunology, Institute of Microbiology, Chinese
filariasis throughout China was certified in 2007 by WHO. Academy of Sciences, Beijing 100101, China (GFG)
Furthermore, the goal of nationwide malaria elimination [email protected]
by 2020 was established, and schistosomiasis is close to We declare no competing interests. We thank experts from the Chinese Center
for Disease Control and Prevention (Liping Wang, Qiaohong Liao, Xiang Ren,
being eliminated. Mengjie Geng, Lingjia Zeng, Shan Lu, Xiaofang Wang, Guomin Zhang, Dan Wu,
Additionally, in China, screening of blood donors and Lijuan Zhang, Yan Cui, Lin Pang, Lixia Wang, Daxin Ni, Xiaochun Wang, and
Songwang Wang), and experts from the Beijing Center for Disease Control and
surgical patients for HIV, hepatitis B virus, hepatitis C Prevention (Jiang Wu and Hongyan Lu), who attended the discussion meetings
virus, and syphilis have been successively required since and made contributions to this Comment.

the 1990s, which facilitated the active identification of 1 Wang L, Wang Y, Jin S, et al. Emergence and control of infectious diseases in
China. Lancet 2008; 372: 1598–605.
new and past infections of these pathogens.8,9 However, 2 Yang S, Wu J, Ding C, et al. Epidemiological features of and changes in
further studies are needed to assess actual incidence incidence of infectious diseases in China in the first decade after the SARS
outbreak: an observational trend study. Lancet Infect Dis 2017; 17: 716–25.
trends. 3 Kim HJ, Fay MP, Feuer EJ, Midthune DN. Permutation tests for joinpoint
regression with applications to cancer rates. Stat Med 2000; 19: 335–51.
As a whole, due to the unprecedented rapid
4 National Bureau of Statistics of the People’s Republic of China. Annual
development of urbanisation and industrialisation national report of statistics. http://www.stats.gov.cn/tjsj/tjgb/ndtjgb/
(accessed July 24, 2017; in Chinese).
in China in the past three decades, the pattern of 5 Cui F, Shen L, Li L, et al. Prevention of chronic hepatitis B after 3 decades of
interaction between human beings and pathogens escalating vaccination policy, China. Emerg Infect Dis 2017; 23: 765–72.
6 Liang X, Bi S, Yang W, et al. Epidemiological serosurvey of hepatitis B in
has changed greatly, substantially altering disease China—declining HBV prevalence due to hepatitis B vaccination. Vaccine
epidemiology. Therefore, to better understand the 2009; 27: 6550–57.
7 Wang L, Utzinger J, Zhou XN. Schistosomiasis control: experiences and
epidemiological features, changing trends, and severity lessons from China. Lancet 2008; 372: 1793–95.
of diseases, a well functioning public health surveillance 8 Li L, Li KY, Yan K, et al. The history and challenges of blood donor screening
in China. Transfus Med Rev 2017; 31: 89–93.
system, integrated with population-based studies on 9 Song Y, Bian Y, Petzold M, Ung CO. Prevalence and trend of major
specific diseases, should be continually intensified to transfusion-transmissible infections among blood donors in western
China, 2005 through 2010. PLoS One 2014; 9: e94528.
effectively plan, implement, evaluate, and improve

Threats of vector-borne zoonotic disease in Europe:


dogs, drosophilids, and Oriental eye worm
Mosquito and tick ecology has changed in parts of Europe During the past 20 years, cases of human and canine
over the past 20 years and threats to the UK from diseases visceral leishmaniasis (caused by the protozoan
such as dengue, West Nile virus, tick-borne encephalitis, and Leishmania infantum, which is transmitted by sandflies)
Crimean-Congo haemorrhagic fever have to be considered.1 have increased throughout historical endemic foci
But health professionals must also be aware of increasing in coastal Mediterranean regions. Furthermore, the
risks from less well known vector-borne zoonoses that disease has spread beyond these regions into new areas
have emerged in Europe during the same timeframe. These at more northerly latitudes, including northern Italy2
zoonotic conditions include certain parasitic disorders of and Madrid, Spain.3 Like visceral leishmaniasis, canine
dogs that are well known to veterinarians, such as visceral dirofilariasis, which is caused by mosquito-transmitted
leishmaniasis and dirofilariasis. However, it is the spread of filarial worms, is also often diagnosed in southern
an apparently new disease that affects the eyes, thelaziosis, Mediterranean regions. Until 1999, most cases in
which we wish to highlight. human beings originated from Italy, France, Greece,

www.thelancet.com/infection Vol 17 November 2017 1115


Comment

west to east, possibly via the ranging behaviour of


A B C
foxes, and it appears to be the same haplotype of the
parasite, which is distinct from the Asian varieties,
that is presently circulating, most recently recorded in
Greece.10
This emerging pattern of thelaziosis is not explained
simply by increased awareness and surveillance.
Changes in patterns of all zoonotic vector-borne
diseases are multifactoral,1 with both animal and
human movement playing a part. In the UK and
other non-endemic countries in Europe, diseases
such as dirofilariasis and visceral leishmaniasis are
Figure: Features of Thelazia callipaeda
(A) An adult female Thelazia callipaeda, measuring 1·1 cm, that was removed from the eye of a Chinese student in
well documented in dogs that have travelled, and in
the UK. (B) Typical six-sided mouth or buccal cavity and the striated cuticle of the worm. (C) Larvae within the worm this way, dogs provide a potential source of parasites
uterus.
to existing and competent vectors in waiting. In the
and Spain, but the pattern of this disease has also case of the UK, ticks, mosquitoes, and Phortica spp
changed, with autochthonous cases now regularly await the annual return of some 200 000 pets that
being reported from northern, central, and eastern have been taken abroad, and the increasing numbers
Europe.4 of animals being imported illegally from eastern
Of special note, however, is thelaziosis caused by Europe. Earlier this year, we described the first cases
the spiruroid nematode Thelazia callipaeda. Unknown of thelaziosis in the UK in dogs that had travelled,11
in Europe until only 25 years ago, thelaziosis is highly one from Romania, the others from France and Italy,
unusual in parasitology in that male fruit flies (Phortica and also investigated an unrelated case of thelaziosis
spp, family Drosophilidae) are the vectors,5 and in a human being. This case involved a Chinese
transmission occurs when larvae are deposited as the national from Beijing who arrived in October, 2016,
fly feeds on lacrimal secretions. Adult worms develop to study at a UK University, and was probably infected
within the conjunctival sacs and lacrimal glands, during stays in rural areas of Mongolia in June of that
and clinical outcomes range from asymptomatic year. Symptoms started soon after arrival in the form
carriage to conjunctivitis, corneal ulceration and, if of severe discomfort with a foreign body sensation,
left untreated, blindness.6 From its first description in and the patient reported seeing worms in one eye.
Beijing 100 years ago,7 T callipaeda has been known However, although they remained undetected on
as Oriental eye-worm because of its distribution two visits to an eye hospital in January, which lead to
across Asia and the Indian subcontinent, where it is suspicion of delusional parasitosis, worms were finally
recognised as an emerging problem; more than 1000 recovered on the third consultation several weeks
confirmed cases in human beings have been recorded later (figure).
in the past 20 years.8 In central China, this neglected While certain notorious and invasive mosquito vectors
disease is prevalent wherever dogs are found, and of major diseases quite rightly occupy the public health
predictably affects mainly elderly people, children, centre stage, it is important to appreciate the problems
and other vulnerable individuals in poorer rural areas. presented by other lower profile but still serious
In Europe, T callipaeda was first diagnosed in domestic vector-borne disorders. Thelaziosis offers a differential
dogs in Italy in 19899 and since then has been diagnostic challenge to distinguish it from allergic
reported in dogs, cats, and wildlife in many countries factors and other pathogens, including include various
in Europe. Eight human cases have been described aberrant helminths.6 The way forward to address these
so far, from Italy, France, Spain, and, only last year, challenges is through a multidisciplinary one-health
the Balkan states, in addition to increasing reports of effort as we here demonstrate through collaborative
infections in domestic dogs in previously unaffected liaison, an approach essential to combat all vector-borne
countries. In fact, the worm seems to be moving from diseases.

1116 www.thelancet.com/infection Vol 17 November 2017


Comment

*John W McGarry, John Graham-Brown, Monika Pasztor 4 Simón F, Siles-Lucas M, Morchón R, et al. Human and animal dirofilariasis:
Department of Pathology and Public Health, Institute of the emergence of a zoonotic mosaic. Clin Microbiol Rev 2012; 25: 507–44.
5 Máca J, Otranto D. Drosophilidae feeding on animals and the inherent
Veterinary Science (JWM), and Department of Infection Biology, mystery of their parasitism. Parasit Vectors 2014; 7: 516.
Institute of Infection and Global Health (JG-B), University of 6 Otranto D, Eberhard M. Zoonotic helminths affecting the human eye.
Liverpool, Liverpool L3 5RF, UK; and Morecambe Bay Hospitals Parasit Vectors 2011; 4: 41
NHS Trust, Microbiology Department, Royal Lancaster Infirmary, 7 Stuckey E. Circumocular filariasis. Br J Ophthalmol 1917; 1: 542–46.
8 Shen J, Gasser R, Chu D, et al. Human thelaziosis—a neglected parasitic
Lancaster, UK (MP) disease of the eye. J Parasitol 2006; 92: 872–75.
[email protected] 9 Rossi L, Bertaglia P. Presence of Thelazia callipaeda Railliet & Henry, 1910, in
We declare that we no conflicts of interests Piedmont, Italy. Parassitologia 1989; 31: 167–72.
10 Papadopoulos E, Komnenou A, Thomas A, Loannidou E, Colella V,
1 Medlock J, Leach S. Effect of climate change on vector-borne disease risk in Otranto D. Spreading of Thelazia callipaeda in Greece. Transbound Emerg Dis
the UK. Lancet Infect Dis 2015; 15: 721–30. 2017; published online Feb 26. DOI: 10.1111/tbed.12626.
2 Varani S, Cagarelli R, Melchionda F, et al. Ongoing outbreak of visceral 11 Graham-Brown J, Gilmore P, Colella V, et al. Three cases of imported
leishmaniasis in Bologna Province, Italy, November 2012 to May 2013. eyeworm infection in dogs: a new threat for the UK. Vet Rec 2017;
Euro Surveill 2013; 18: 20530. published online Sept 4. DOI:10.1136/vr.104378.
3 Arce A, Estirado A, Ordobas M, et al. Re-emergence of leishmaniasis in
Spain: community outbreak in Madrid, Spain, 2009 to 2012.
Euro Surveill 2013; 18: 20546.

Corrections
Saunders MJ, Wingfield T, Tovar MA, et al. A score to predict and stratify risk of
tuberculosis in adult contacts of tuberculosis index cases: a prospective Published Online
derivation and external validation cohort study. Lancet Infect Dis 2017; 17: September 13, 2017
1090–99—The support and grants in the Acknowledgments section should http://dx.doi.org/10.1016/
have been assigned as follows: This study was supported by Wellcome S1473-3099(17)30573-X
Trust awards 057434/Z/99/B (MAT, KZ, RM, TRV, JSF, RHG, and CAE),
Z070005/Z/02/Z (MAT, TRV, JSF, RHG, and CAE), 078340/Z/05/Z (MAT, KZ,
RM, TRV, JSF, and RHG, CAE), 105788/Z/14/Z (SD, RHG, and CAE),
201251/Z/16/Z (MJS, RHG, and CAE), the Department for International
Development Civil Society Challenge Fund (MAT, KZ, RM, TRV, CAE), the
Joint Global Health Trials consortium (Medical Research Council,
Department for International Development, and Wellcome Trust award
MR/K007467/1 [TW, MAT, KZ, RM, TRV, RHG, and CAE]), the Bill & Melinda
Gates Foundation (award OPP1118545 [TW, MAT, RM, TRV, and CAE]),
Imperial College National Institutes of Health Research Biomedical
Research Centre (JAF and CAE), the Foundation for Innovative New
Diagnostics (MAT, KZ, TRV, and CAE), the Sir Halley Stewart Trust (CAE),
WHO (CAE), the STOP TB partnership’s TB REACH initiative funded by the
Government of Canada (W5_PER_CDT1_PRISMA [MAT, RM, and CAE]),
and Innovation For Health And Development (MJS, TW, and CAE). This
correction has been made to the online version as of Sept 13, 2017, and the
printed Article is correct.

www.thelancet.com/infection Vol 17 November 2017 1117

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