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1 s2.0 S0001706X1830980X Main
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Acta Tropica
journal homepage: www.elsevier.com/locate/actatropica
A R T I C LE I N FO A B S T R A C T
Keywords: Cystic echinococcosis (CE) is a global parasitic zoonosis for which ultrasound (US) is the gold standard modality
Cystic echinococcosis for diagnosis. In 2003, the WHO published a standardized US classification of CE, on which WHO treatment
Ultrasound guidelines are based. In 2014, global adoption of the classification was questioned by a publication which
Classification indicated that, between 2004 and 2014, only half of studies utilizing a classification used the WHO classification.
More recent studies have demonstrated that the WHO classification best reflects the natural history of CE, and is
used with high reliability by experts in the field; despite these attributes, the classification’s impact is ultimately
limited by the extent of its adoption. A PubMed search using the terms “Echinococcus granulosus ultrasound,”
“Echinococcus granulosus classification,” “cystic echinococcosis ultrasound,” and “cystic echinococcosus clas-
sification” revealed publications on human CE utilizing a US classification. Classification(s) used, year of pub-
lication, and the country of the first author’s institution were recorded. From 2004 to 2010, the WHO classifi-
cation was used in 50% or fewer of included publications for 6 of the 7 years. After 2011, it appeared in a low of
75% (2013) to a high of 96% (2017) of included publications. Of all included studies published from 2004 to
2017, the WHO classification was referenced in 18% (3 of 17) from Africa, 64% (32 of 50) from Asia, 79% (89 of
113) from Europe, 89% (8 of 9) from North America, and 100% (9 of 9) from South America. Findings suggest
that the WHO classification has been progressively taking preference to other classifications, with rate of
adoption depending on continent of origin of the research. Residual use of the classification developed by Dr.
Hassen Gharbi of Tunisia in 1982, used widely prior to development of the WHO classification (which reversed
two stages in Gharbi’s classification in order to more closely reflect the natural history of CE) suggests that
adoption of a new classification takes time and varies regionally.
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Corresponding author at: St. George’s University School of Medicine, P.O. Box 7, St. George, Grenada.
E-mail addresses: emirabil@sgu.edu (E. Mirabile), nsolomon@sgu.edu (N. Solomon), pfields@sgu.edu (P.J. Fields), cmacpherson@sgu.edu (C.N.L. Macpherson).
1
St. George’s University, P.O. Box 7, St. George, Grenada.
https://doi.org/10.1016/j.actatropica.2018.09.024
Received 19 August 2018; Accepted 25 September 2018
Available online 27 September 2018
0001-706X/ © 2018 Published by Elsevier B.V.
E. Mirabile et al. Acta Tropica 189 (2019) 6–9
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E. Mirabile et al. Acta Tropica 189 (2019) 6–9
Table 3 CE3A cysts. For CE4 and CE5 cysts, the “wait and watch” approach is
US classification utilization by country. recommended (Brunetti et al., 2010). Pharmacological treatment al-
Publications by Country of First Author’s Affiliated Institution ready operates at relatively low success rates and becomes even less
successful as cysts become more complex; as such, providing che-
Country Frequency Percent motherapy in an inappropriate stage of disease further reduces treat-
ment efficacy (Brunetti et al., 2010; Gil-Grande et al., 1993).
Argentina 5 2.5
Austria 1 0.5 Because of the dependence of parasite eradication on proper diag-
Bangladesh 1 0.5 nosis and staging, international adoption of the WHO classification is
Bulgaria 2 1.0 vital for establishing best clinical practices and optimizing patient care.
China 19 9.6 Despite initial concerns that the WHO classification would not super-
Denmark 1 0.5
sede Gharbi’s, present observations suggest that the WHO classification
Finland 1 0.5
France 1 0.5 has been progressively taking preference. From 2004 through 2011,
Germany 16 8.1 Gharbi’s classification appeared to predominate; the past six years,
Grenada 4 2.0 however, have reflected a very different situation. From 2004 to 2010,
India 14 7.1
the WHO classification was used in 50% or fewer of included publica-
Iran 4 2.0
Italy 31 15.7
tions for 6 of the 7 years. After 2011, it appeared in a low of 75% (2013)
Japan 4 2.0 to a high of 96% (2017) of included publications. Of all included studies
Kenya 1 0.5 published from 2004 to 2017, the WHO classification was referenced in
Korea 2 1.0 18% (3 of 17) from Africa, 64% (32 of 50) from Asia, 79% (89 of 113)
Latvia 1 0.5
from Europe, 89% (8 of 9) from North America, and 100% (9 of 9) from
Morocco 8 4.0
Netherlands 1 0.5 South America.
Pakistan 2 1.0 These findings suggest that the WHO classification has been pro-
Palestine 1 0.5 gressively taking preference to other classifications, with rate of
Peru 4 2.0
adoption depending on the continent of origin of the research and/or
Poland 3 1.5
Portugal 2 1.0
researchers. Residual use of the classification developed by Dr. Hassen
Saudi Arabia 2 1.0 Gharbi of Tunisia in 1982, used widely prior to development of the
Spain 6 3.0 WHO classification (which reversed two stages in Gharbi’s classification
Switzerland 3 1.5 in order to more closely reflect the natural history of CE) suggests that
Taiwan 1 0.5
adoption of a new classification takes time and varies regionally.
Tunisia 8 4.0
Turkey 40 20.2 The community of clinicians and researchers studying CE is very
UK 3 1.5 small, even compared to those studying many other parasitic and non-
Ukraine 1 0.5 parasitic neglected tropical diseases. Given the wide geographical dis-
USA 5 2.5
tribution of CE, it is not surprising that these researchers also hail from
Total 198 100.0
around the globe and speak a multitude of different languages. Because
of this, it is enormously important that the few who are investigating
activity and correlate with US appearance, accurate staging is para- this disease are able to communicate their findings clearly and effec-
mount for determining and administering appropriate treatment. The tively. Use of a common classification system facilitates communication
most recent guidelines developed by the WHO Informal Working Group and understanding between these researchers by providing a common
on Echinococcosis (IWGE) suggest surgery for removal of CE2 and CE3B language to discuss important features of CE—including epidemiology,
cysts, puncture-aspiration-injection-reaspiration (PAIR) for removal of diagnosis, and management—and share new findings. In this way, more
large (> 5 cm) CE1 and CE3A cysts, and chemotherapy (typically the efficient communication ultimately allows for more effective clinical
benzimidazole carbamate albendazole) for small (< 5 cm) CE1 and and research practices.
This study’s use of PubMed searches to identify articles is limited in
8
E. Mirabile et al. Acta Tropica 189 (2019) 6–9
Fig. 2. Demonstration of classification use by year and continent, from 2004 to 2017.
that there may be other articles in journals not listed on PubMed which Brunetti, E., Kern, P., Vuitton, D.A., 2010. Expert consensus for the diagnosis and treat-
use one or any number of these classifications. The PubMed database ment of cystic and alveolar echinococcosis in humans. Acta Trop. 114 (1), 1–16.
Gil-Grande, L.A., et al., 1993. Randomised controlled trial of efficacy of albendazole in
was chosen specifically for its high volume of peer-reviewed publica- intra-abdominal hydatid disease. Lancet 342 (8882), 1269–1272.
tions from national and international journals which are both easily Kern, P., 2003. Echinococcus granulosus infection: clinical presentation, medical treat-
accessible to the scientific community and receive international atten- ment and outcome. Langenbecks Arch. Surg. 388 (6), 413–420.
Macpherson, C.N., 1992. Ultrasound in the diagnosis of parasitic disease. Trop. Doct. 22
tion purely by nature of being listed within this database. We feel use of (1), 14–20.
PubMed therefore provides an accurate representation of current trends Macpherson, C.N., Milner, R., 2003. Performance characteristics and quality control of
within the field. community based ultrasound surveys for cystic and alveolar echinococcosis. Acta
Trop. 85 (2), 203–209.
It remains to be seen if complete adoption in those regions still
Macpherson, C.N., et al., 1987. Portable ultrasound scanner versus serology in screening
showing a degree of allegiance to Gharbi’s classification will eventually for hydatid cysts in a nomadic population. Lancet 2 (8553), 259–261.
occur, at a slower rate or at all. Given recent studies establishing the Pawłowski, Z.S., et al., 2001. Echinococcosis in humans: clinical aspects, diagnosis and
treatment, in WHO/OIE manual on echinococcosis in humans and animals: a public
WHO standardized classification of CE as the US classification most
health problem of global concern. In: Eckert, J. (Ed.), World Organisation for Animal
closely following disease natural history, and in the interest of estab- Health (Office International des Epizooties), editors. World Health Organization:
lishing a universal language to discuss this disease, continued turnover Paris, France, Paris, France, pp. 20–72.
and widespread adoption of this classification should be promoted. Solomon, N., et al., 2017a. Cystic echinococcosis in Turkana, Kenya: the role of cross-
sectional screening surveys in assessing the prevalence of human infection. Am. J.
Future investigations might question what effect adoption of the WHO Trop. Med. Hyg. 178, 182–189.
classification and the subsequently developed treatment guidelines Solomon, N., et al., 2017b. Expert reliability for the world health organization standar-
have had on treatment outcomes; and whether there is a difference in dized ultrasound classification of cystic echinococcosis. Am. J. Trop. Med. Hyg. 96
(3), 686–691.
treatment outcomes depending on the tool used to classify disease Solomon, N., et al., 2017c. The natural history of cystic echinococcosis in untreated and
stage. albendazole-treated patients. Acta Trop. 171, 52–57.
Symeonidis, N., et al., 2013. Complicated liver echinococcosis: 30 years of experience
from an endemic area. Scand. J. Surg. 102 (3), 171–177.
Acknowledgments Tamarozzi, F., et al., 2014. Acceptance of standardized ultrasound classification, use of
albendazole, and long-term follow-up in clinical management of cystic echino-
The authors would like to thank Dr. Francesca Tamarozzi for sup- coccosis: a systematic review. Curr. Opin. Infect. Dis. 27 (5), 425–431.
Thompson, R.C.A., McManus, D.P., et al., 2001. Aetiology: parasites and life cycles. In:
porting this study and assisting the authors in commencing it. No Eckert, J. (Ed.), Who/Oie Manual on Echinococcosis in Humans and Animals: A
funding was required for this study. Public Health Problem Of Global Concern. World Organisation for Animal Health
(Office International des Epizooties) Paris, France, World Health Organization, Paris,
France, pp. 1–19.
References
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coccosis for application in clinical and field epidemiological settings. Acta Trop. 85
Belard, S., et al., 2015. Point-of-Care ultrasound assessment of tropical infectious (2), 253–261.
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