International Journal of Infectious Diseases
Volume 15, Issue 9 , Pages e611-e619, September 2011

Europe's neglected infections of poverty

  • Peter J. Hotez

      Affiliations

    • Sabin Vaccine Institute and Section of Pediatric Tropical Medicine, National School of Tropical Medicine at Texas Children's Hospital and Baylor College of Medicine, Houston, Texas, USA
    • Corresponding Author InformationCorresponding author. Tel.: +1 202 841 3020.
  • ,
  • Meredith Gurwith

      Affiliations

    • Georgetown University, Washington DC, USA

Received 1 November 2010; received in revised form 20 March 2011; accepted 6 May 2011. published online 15 July 2011.

Corresponding Editor: William Cameron, Ottawa, Canada.

Article Outline

Summary 

Objectives

To review the prevalence, incidence, and geographic distribution of the major neglected infections of poverty in Europe as a basis for future policy recommendations.

Methods

We reviewed the literature from 1999 to 2010 for neglected tropical diseases listed by PLoS Neglected Tropical Diseases (http://www.plosntds.org/static/scope.action) and the geographic regions and countries of (continental) Europe. Reference lists of identified articles and reviews were also hand searched, as were World Health Organization databases.

Results

In Eastern Europe, the soil-transmitted helminth infections (especially ascariasis, trichuriasis, and toxocariasis), giardiasis, and toxoplasmosis remain endemic. High incidence rates of selected food-borne helminthiases including trichinellosis, opisthorchiasis, taeniasis, and echinococcosis also occur, while brucellosis and leptospirosis represent important bacterial zoonoses. Turmoil and economic collapse following the war in the Balkans, the fall of Communism, and Europe's recent recession have helped to promote their high prevalence and incidence rates. In Southern Europe, vector-borne zoonoses have emerged, including leishmaniasis and Chagas disease, and key arboviral infections. Additional vulnerable populations include the Roma, orphans destined for international adoption, and some immigrant groups.

Conclusions

Among the policy recommendations are increased efforts to determine the prevalence, incidence, and geographic distribution of Europe's neglected infections, epidemiological studies to understand the ecology and mechanisms of disease transmission, and research and development for new control tools.

Keywords: Neglected infections of poverty, Helminth infections, Zoonoses, Toxoplasmosis, Roma, International adoption

 

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1. Introduction 

The phrase ‘neglected tropical diseases’ refers to a group of chronic and debilitating parasitic infections, as well as related bacterial, fungal, and viral infections, affecting hundreds of millions of people living in low- and middle-income countries.1 In such developing regions of the world, the neglected tropical diseases have been shown to actually trap the poor in a vicious cycle of poverty because of the tendency of these infections to impair child development, pregnancy outcome, and worker productivity.2 Recently, it was shown that a similar group of parasitic and other diseases, known as the ‘neglected infections of poverty’ are also widespread among the poor living in some wealthy countries such as the USA,3 and there is a rationale for looking at poverty as a key determinant for these health disparities worldwide.4, 5, 6 Given Europe's recent economic downturn in the setting of approximately 20 years of economic fragility that resulted from war in the Balkans, the fall of communism, and the break-up of the former Soviet Union, it was pointed out that neglected infections of poverty may be highly prevalent in Europe, but especially in Eastern and Southern Europe and in Turkey, where the living standards are the lowest and the economies remain weak.6 Here we review the prevalence, incidence, and geographic distribution of Europe's major neglected infections of poverty and then outline initial steps for formulating health policy recommendations for these conditions.

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2. Methods 

The review of the literature (papers or abstracts in English only) was conducted using the online database PubMed for the last 11 years (1999–2010) using the specific diseases listed as neglected tropical diseases on the PLoS Neglected Tropical Diseases website (http://www.plosntds.org/static/scope.action) and the geographic regions and countries of (continental) Europe as the Medical Subject Headings (MeSHs). Reference lists of identified articles and reviews were also hand searched as were databases from the World Health Organization (http://www.who.int).

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3. Results 

3.1. Europe's East–West gap and vulnerable populations 

With more than 700 million people, Europe is the third most populous continent (after Asia and Africa), and its roughly 50 states together represent the world's largest economy.7 However, while Europe is undeniably an economic powerhouse, this fact alone belies a complicated misdistribution of wealth on the continent. Just as there is a hidden underbelly of poverty in the Mississippi Delta, along the border with Mexico, and in the inner cities of the USA, so too does great poverty lurk in Europe. As many as 165 million people in Europe (more than 20% of the population) live below poverty thresholds and approximately 2% of the European population lives in absolute poverty.8

Even among the 27 countries of the European Union (EU), which over-represents the wealthier countries, an estimated 16% of citizens or almost 80 million people live below the poverty threshold, defined as 60% of their country's median income. Additionally, almost 20% of the EU's children live in poverty.9, 10, 11 Poverty in Europe is distributed along a fairly well-defined gradient. Listed in Table 1 is the gross domestic product (GDP) per capita for each European nation (estimated in 2008), organized into four quartiles. Most of the countries in the top two quartiles are Western European nations, while the third and fourth, or poorest quartiles, contain exclusively Eastern European nations. Countries located in Europe's southeastern region represent the lowest tier. Figure 1 pictorially represents this situation, with almost all the lowest GDP per capita countries located in the East. As described below, the poverty gap between East and West12 provides a paradigm for understanding the high disease burden from neglected infections in Eastern Europe. While disease burdens in tropical areas may be higher, these infections in Europe suffer from a similar neglect found in poorer countries.13 While some of these infections occur not only among those living in poverty but also among the well-off in Europe, there is a greater disease prevalence in countries with lower GDPs and those at risk are more likely to be poor. These inequalities exist despite the European Convention of Human Rights’ (ECHR) affirmation of a right to life to all people in Europe, since its establishment in 1953.14 The supranational ECHR has been adopted by all 47 members of the Council of Europe, whose members cover almost every European state.

Table 1. Gross domestic product per capita (2008) of European countries, current pricesa
Countries in first quartile, $47 107–$113 044Countries in second quartile, $20 202–$48 016Countries in third quartile, $8502–$17 630Countries in fourth quartile, $1809–$6856
LuxembourgFranceSlovak RepublicBulgaria
NorwayGermanyEstoniaSerbia
SwitzerlandUKCroatiaBelarus
DenmarkItalyHungaryAzerbaijan
IrelandSpainLatviaMacedonia
IcelandCyprusLithuaniaBosnia and Herzegovina
SwedenGreecePolandAlbania
NetherlandsSloveniaRussiaUkraine
FinlandPortugalTurkeyArmenia
AustriaCzech RepublicRomaniaGeorgia
BelgiumMaltaKazakhstanMoldova
Montenegro

aInternational Monetary Fund, World Economic Outlook Database, April 2009.

Among the Eastern European nations, two groups stand out for their extreme poverty and disease burden resulting from neglected infections. First, some of the countries located in Southeastern Europe, including the Balkan nations of Albania, Bosnia and Herzegovina, Bulgaria, Croatia, Kosovo, Macedonia, Montenegro, and Serbia, and Romania, as well as Turkey, are considered Europe's poorest nations and have arguably suffered the greatest devastation over the last two decades.15 The violence from conflict in this region during the 1990s was considered the worst in Europe since the Second World War, and killed hundreds of thousands of people, while leaving tens of thousands permanently disabled or psychologically devastated, and producing vast numbers of refugees who experienced high rates of malnutrition, communicable diseases, and ectoparasitic infestations (i.e., lice and scabies).16, 17 The war also destroyed many healthcare and educational systems.16 A second group of nations made conspicuous by their extreme poverty and disease includes some of the former Soviet bloc countries in Europe, i.e., Belarus, Azerbaijan, Ukraine, Georgia, and Moldova, where the social and health infrastructures were severely affected by the fall of Communism. Both Southeastern Europe and the former Soviet bloc countries may have also suffered disproportionately from unemployment and premature deaths from internal violence occurring in the economic downturn and recession of 2008–2009.18

In addition to the two populations living in the Balkans and the former Soviet bloc countries in Europe, there are three other European populations who require consideration for their vulnerability to high rates of neglected infections. The Roma are an ethnic minority of northern Indian origin who have inhabited Europe since the 11th Century.19 Most of the estimated 7–9 million Roma currently live in Central and Eastern Europe, with the largest number in Romania, followed by Bulgaria, but as a group they also account for over 8% of the population in Macedonia and Slovakia.20 The Roma have disproportionately suffered from the economic hardships following the fall of Communism, in addition to high unemployment. Between 70% and 80% of the Roma in Bulgaria and Romania live in poverty, defined at a level of $4.30 purchasing power parity per capita per day, and are forced to survive in conditions of poor housing, inadequate sanitation, and malnutrition.20 High exposure to intestinal parasites, bacteria, and viruses are of particular concern, and a high prevalence of giardiasis, shigellosis and salmonellosis, and hepatitis A, respectively, have been reported,19, 21, 22 as well as selected respiratory and ectoparasitic infestations, especially pediculosis.19 Roma children also experience low vaccination coverage rates and an increased susceptibility to otherwise preventable childhood infections.19, 23

In addition to the Roma, Europe has one of the world's largest populations of immigrants,24 including migrants from Africa25, 26 who are at risk for high rates of neglected infections, as well as orphans destined for international adoption who suffer from many of the conditions also noted among the Roma.27 The neglected infections of poverty thrive in this setting of conflict, social and political unrest, and discrimination.

3.2. Helminthic neglected infections 

The major helminth infections in Europe include both important soil-transmitted helminth infections caused by parasitic nematodes, as well as food-borne helminthiases and larval cestode infections. Most of these infections are found in Eastern Europe and in Turkey. Among the soil-transmitted helminth infections, ascariasis (intestinal roundworm infection) and trichuriasis (whipworm) are two of the most common infections in low-income countries.1 As shown in Table 2, ascariasis and trichuriasis are still prevalent among children and adults living in the Southeastern European nations of Albania28 and Armenia,29 and among children in Poland.30, 31, 32 The highest published prevalence is in Turkey where it is associated with extreme poverty and poor sanitation.33 Enterobiasis (pinworm infection) is also common throughout Eastern Europe and Turkey,29, 31, 32, 34, 38 and it is present in Italy.39

Table 2. Soil-transmitted helminth infections in Europe
Neglected infectionCountry (and economic quartile)Special populations studiedPrevalence [Ref.]
AscariasisAlbania (4th)Adults and children1% [28]
Armenia (4th)Adults and children4% [29]
Poland (3rd)Children15% [30]; 3% [31]; 1% [32]
Turkey (3rd)Adults and children69% [33]
TrichuriasisAlbania (4th)Adults and children12% [28]
Armenia (4th)Adults and children1% [29]
Poland (3rd)Children8% [31]; <1% [32]
Turkey (3rd)Adults and children65% [33]
EnterobiasisArmenia (4th)Adults and children26% [29]
Estonia (3rd)Preschool children23% [34]
Italy (2nd)Children13% [39]
Poland (3rd)Adults and children40% [31]; 38% [35]; 15% [32]; 2% [36]
Turkey (3rd)Children10% [37]; 5% [38]
ToxocariasisHungary (3rd)Children with chronic cough and asthma32% [40]
Poland (3rd)Children10–31% [42]
Adults and childrenNot specified [43]
Slovenia (2nd)Adults and children with ocular disease28% [44]
Turkey (3rd)Rural children17% [45]
Mentally disabled children19% [46]
Adults with asthma13% [47]
Adults with schizophrenia46% [48]
StrongyloidiasisFrance (2nd)Adults and childrenNot determined [49]
Spain (2nd)Adults12% 50, 51

Toxocariasis is a zoonotic helminthiasis from dogs and cats associated with several larval migrans syndromes; it may be the most common human helminth infection in the USA.3 Toxocariasis is also extremely common in Eastern Europe where the seroprevalence for Toxocara-specific antibodies (typically indicative of current or past exposure) ranges between 10% and 32%,40, 41, 42, 43 and where some investigative efforts in Eastern Europe have attempted to link active Toxocara infection to chronic cough and asthma40 and ocular disease.44 In Poland, Toxocara infection of the central nervous system is sometimes referred to as neurotoxocariasis.43 The seroprevalence of Toxocara infection is also high in Turkey, ranging from 13% to 46%.45, 46, 47 Investigative efforts there have also attempted to link this condition to asthma47 and mental disability.46, 48 Finally, in Spain and southwestern France a small focus of human strongyloidiasis has been described,49, 50, 51 especially among elderly male farmers in the region.51Among the food-borne helminthic infections (Table 3), trichinellosis is the most common nematode infection and it is now widespread in Eastern Europe. Pozio52 and Cuperlovic et al.53 have each linked the emergence or re-emergence of trichinellosis in the former Soviet bloc countries and the Balkans to widespread breakdowns in veterinary public health services that resulted from economic collapse associated with the fall of Communism or conflict, respectively. In Romania, the breakdown of large scale abattoirs post-Communism led to an increase in the incidence of trichinellosis as pig slaughtering moved to small farms in poor rural communities.54 As a result, the prevalence of Trichinella infection among swine herds in many rural villages is up to 50%, and the disease has also emerged among game animals.52 In Latvia, Lithuania, Poland, and Russia, outbreaks of trichinellosis resulting from the consumption of uncooked pork or wild boar meat have been reported.55, 56, 57, 58

Table 3. Food-borne and other zoonotic helminth infections in Europe
Neglected infectionCountry (and economic quartile)Special populations studied or specific commentsPrevalence, incidence, or number of cases [Ref.]
TrichinellosisBelarus (4th)Swine herds≤50% [52]
Croatia (3rd)
Latvia (3rd)
Lithuania (3rd)
Romania (3rd)
Russia (3rd)
Serbia (4th)
Ukraine (4th)
Bulgaria (4th)Re-emergence with social and political systems and conflictHigh prevalence in humans and domestic animals [53]
Serbia (4th)
Montenegro (4th)
Romania (3rd)
Croatia (3rd)
Latvia (3rd)2005 outbreak from baconNot specified [55]
Lithuania (3rd)Not specifiedNot specified [56]
Poland (3rd)2006 outbreaks from wild boar meat130 cases [57]
Russia (3rd)2003–2004 outbreaks from porkNot specified [58]
OpisthorchiasisCountries of the former Soviet Union>35 species of freshwater fish12.5 million people at risk [59]
Belarus (4th)Brest, Gomel, Grodno provincesNot specified [60]
Italy (2nd)Central Italy (Lake Trasimeno)Two outbreaks in 2003 and 2005 [61]
Russia (3rd)Ob and Irtysh river valleys40–95% prevalence [60]
Ukraine (4th)Dnieper River basin5–40% prevalence [60]
FascioliasisTurkey (3rd)Sporadic case reportsNot specified 62, 63
Spain (2nd)
France (2nd)
Portugal (2nd)
TaeniasisPoland (3rd)Taenia saginata is the most common intestinal cestode in Poland157 registered cases in 2003 [64]; high prevalence in Eastern Europe [65]; prevalence in Western Europe 0.01–2% [66]; Taenia solium has been eradicated [67]
Cystic echinococcosisBulgaria (4th)Possible re-emergenceIncidence of 3.3 per 100 000 [68]
Poland (3rd)Not specified34 registered cases in 2003 [64]
Slovenia (2nd)Prevalence has decreased since the 1960s1.7 per 105 inhabitants [69]
Spain (2nd)Most affected regions are northeastern, central, western parts of the countryIncidence of 1.1–3.4 cases per 100 000 [70]
Turkey (3rd)Serious public health problem in Turkey2.7% seroprevalence rate in Central Anatolia [71]
Serbia (4th)Pediatric surgical patientsNot specified [72]
Alveolar echinococcosisCentral and Eastern EuropeLinked with increases in fox populationsLow incidence rates [73]
Germany (2nd)Northern province of Lower SaxonyPrevalence among red foxes increase to 8.5% [74]
Lithuania (3rd)Not specifiedNot specified [75]
Slovak Republic (3rd)Not specifiedHigh prevalence in dogs [76]
Slovenia (2nd)Not specifiedIncidence of 0.45 per 100 000 [77]
Switzerland (1st)Increase in incidenceIncidence of 0.26 per 100 000 [78]

Keiser and Utzinger59 estimate that 12.5 million people living in countries of the former Soviet Union are at risk for opisthorchiasis, a liver fluke infection caused by ingesting freshwater fish infected with encysted metacercariae of Opisthorchis felineus.59 High prevalence rates of opisthorchiasis have been reported from Belarus, Russia, Kazakhstan, and Ukraine, with the highest rates in western Siberia where the prevalence can reach 95%.60 Another form of opisthorchiasis caused by Opisthorchis viverrini occurs in Southeast Asia, but chronic infections with either species can cause cholangiocarcinoma (bile duct cancer).60 As a result, cholangiocarcinoma is a major public health problem in the affected areas of Russia and elsewhere. Recently, a small outbreak of opisthorchiasis was reported from Italy due to the consumption of infected fish from Lake Trasimeno.61 Sporadic cases of fascioliasis, a zoonotic liver fluke infection associated with sheep herding, has been reported from Turkey and in Southern Europe, especially northern Spain, Portugal, and France (mostly in the southwestern region).59, 62, 63

The beef tapeworm, Taenia saginata, is the most common intestinal cestode in Poland,64 and is considered common in Eastern Europe,65 but with a far lower prevalence in Western Europe (as low as 0.01%).66 In contrast, the pork tapeworm Taenia solium has been eradicated from Poland,67 although the overall prevalence of infection with this parasite as well as cysticercosis in Europe is unknown. Hymenolepiasis has been reported from Albania28 and presumably occurs elsewhere in Eastern Europe. Among the larval cestode infections, cystic echinococcosis occurs commonly in Bulgaria, Poland, Slovenia, and elsewhere in Eastern and Central Europe.64, 68, 69 The infection is also commonly found in Spain70 and it is considered a serious public health problem in Turkey.71 A 17-year review (1990–2006) of pediatric surgical patients at two major pediatric hospitals in Serbia showed that cystic echinococcosis in Serbia remains endemic. The number of infections may be underestimated due to the decline in public health services after 1995 as a result of conflict in the region.72 Alveolar echinococcosis has also emerged in Central and Eastern Europe in association with increases in fox populations.73 The infection has been reported in Germany,74 Lithuania,75 Slovakia,76 Slovenia,77 and Switzerland.78 Because of the unique sylvatic nature of alveolar echinococcosis, it is one of the few helminth infections in Europe that is not linked to poverty and inadequate sanitation.

3.3. Protozoan neglected infections 

Table 4 summarizes the major protozoan infections in Europe. Giardiasis is a common intestinal protozoan infection in Eastern Europe28, 31, 32 and Turkey,37 although its overall health impact on young children, especially preschool children, has not been established. Amebiasis has been reported from Turkey and elsewhere,79 and trichomoniasis is considered an important sexually transmitted protozoan infection,80 but both infections have been vastly under-reported. Among the vector-borne protozoan infections, approximately 700 new cases of leishmaniasis (caused predominantly by the autochthonous species, Leishmania infantum) now occur annually in Southern Europe where it is a zoonosis transmitted from dogs by Phlebotomus sandflies.81, 82 The major affected countries include Portugal, Spain, France, Italy, and Greece,81 as well as Croatia.83 However, 3000 additional cases occur in Turkey,81 especially the Aegean, Mediterranean, and Central Anatolia regions,84 and there is evidence for its emergence north to Germany and Italy.81 A recent review of pediatric visceral leishmaniasis cases in Albania from 1995 to 2009 showed a strong connection between the prevalence of the disease and poverty.85 The incidence of the disease in children and co-morbidities are elevated in comparison to neighboring Mediterranean countries that share the same agents, reservoir, and vectors.85 L. infantum infections are also common in the dog population, which has a seroprevalence of 25%.81 Of concern is the potential for further spread of leishmaniasis because of climate change,82 and the additional emergence of Leishmania donovani (an important cause of visceral leishmaniasis in Asia) into the region, as well as cutaneous leishmaniasis caused by Leishmania tropica,81 which is now common in Turkey.84 As many as 6125 cases of Chagas disease are present in Spain having been introduced there as a result of reverse international migrations from Latin America.86 The infection has also been reported from France.87 There are concerns about contamination of the Southern European blood supply with Trypanosoma cruzi, the causative agent of Chagas disease.

Table 4. Protozoan neglected infections in Europe
Neglected infectionCountry (and economic quartile)Special population examinedPrevalence, incidence, or number of cases [Ref.]
GiardiasisAlbania (4th)Adults and children11% [28]
Poland (3rd)Children1% 31, 32
Turkey (3rd)Adults and children8% [37]
AmebiasisTurkey (3rd)ChildrenNot specified [79]
TrichomoniasisLatvia (3rd)AdultsNot specified [80]
LeishmaniasisPortugal (2nd)Adults and children700 human cases reported annually 81, 82
(visceral and cutaneous)Spain (2nd)
France (2nd)
Italy (2nd)
Greece (2nd)
Cyprus (2nd)
Croatia (3rd)Adults and children35 cases from 1994 to 2006 [83]
Turkey (3rd)Adults and children>3000 human cases reported annually 81, 84
Albania (4th)Children25 in 100 000 in the age group 0–6 years [85]
Chagas diseaseSpain (2nd)Adults and children6125 cases (25 per 1000 of immigrants from Latin America) [86]
France (2nd)Adults and children9 cases from 2004 to 2006 [87]
ToxoplasmosisCentral and Eastern EuropeAdults and childrenIncreasing gradient of adult seroprevalence and congenital infection from West to East [88]
Albania (4th)Pregnant women49% seropositive for IgG; 1% seropositive for IgM [89]
Estonia (3rd)Randomly selected subjects55% seroprevalence for IgG [90]
Iceland (1st)Randomly selected subjects10% seroprevalence for IgG [90]
Poland (3rd)Forestry workers62.5% seroprevalence for IgG; 4% seroprevalence for IgM [91]
Serbia (4th)Women of reproductive ageConsumption of beef as a risk factor [92]
Slovenia (2nd)Pregnant women34% seropositive; 132 with primary infection; 9 per 1000 women at risk for acquiring the primary infection [93]
Sweden (1st)Randomly selected subjects23% seropositive for IgG [90]
Turkey (3rd)Pregnant women in first trimester30% seropositive for IgG [94]

Together with Latin America, the Middle East, Southeast Asia, and Africa, there are regions of Central and Eastern Europe that are considered highly endemic for both acquired and congenital toxoplasmosis.88 In Europe, an increasing gradient of this infection from West to East has been proposed,88 although currently only the nations of France and Germany conduct surveillance screening. High seroprevalence and evidence of congenital Toxoplasma infection have recently been reported from Albania,89 Estonia,90 Poland,91 Serbia,92 and Slovenia,93 as well as in Turkey.94 In Serbia, the infection has been linked primarily to consumption of undercooked beef,92 whereas exposure to soil contaminated with cat feces is the major factor in Estonia,90 and contaminated water in Turkey.94

3.4. Bacterial and viral neglected infections 

The zoonotic bacterial infections brucellosis and leptospirosis have re-emerged in Bulgaria and elsewhere in Eastern Europe, as shown in Table 5.95, 96, 97, 98, 99 Migrant workers from Eastern Europe have also introduced leptospirosis into Germany.100 Among the factors noted for the rise in bacterial zoonoses in Eastern Europe are the socioeconomic changes outlined above, with an increase in animal movement and occupational migration from Greece and Turkey, which are established disease endemic countries.97 Outbreaks of tularemia have also been noted in Bulgaria101 and Sweden,102 while rickettsial diseases and other infections caused by intracellular organisms are endemic to Croatia and elsewhere.103, 104 In the years following the collapse of Communism and the changes in public health infrastructures associated with the break-up of the former Soviet Union, both syphilis and congenital syphilis have emerged in the former Soviet bloc nations of Belarus, Estonia, Kazakhstan, Moldova, and Ukraine, with the number of cases peaking in the late 1990s.105 Since then, a subsequent rise in syphilis has been noted in Western European cities.105

Table 5. Bacterial and viral neglected infections in Europe
Neglected infectionCountry (and economic quartile)Special population examinedPrevalence, incidence, or number of cases [Ref.]
Bacterial infections
BrucellosisBosnia and Herzegovina (4th)Hospitalized patientsSecond most common cause of hospitalized zoonoses [95]
Bulgaria (4th)Not specified105 cases between 2005 and 2007 96, 97
LeptospirosisBulgaria (4th)Primarily adultsIncidence rate of 0.42 per 100 000 population [98]; patients in high-risk group were 20–39 years old, cattle raisers, fisherman, land workers [99]
Germany (2nd)Migrant strawberry harvesters from Eastern Europe16% attack rate [100]
TularemiaBulgaria (4th)Not specifiedLocal outbreaks associated with vector transmission 101, 102
Sweden (1st)
Rickettsial infections and other infections with intracellular bacteriaCroatia (3rd)Not specifiedSporadic infection in Adriatic island and coastal area 103, 104
Syphilis and congenital syphilisRussia (3rd)Heterosexuals and men who have sex with menIncidence of 170 per 100 000 of syphilis in 1996 [105]
Belarus (4th)
Estonia (3rd)
Kazakhstan (3rd)
Moldova (4th)
Ukraine (4th)
Arbovirus infections and other viral diseases
Chikungunya virus infectionItaly (2nd)Not specified205 cases in 2007 106, 107
West Nile fever virus infectionRomania (3rd)Not specifiedNot specified [108]
Bulgaria (4th)
Italy (2nd)
France (2nd)
Crimean-Congo hemorrhagic feverKosovoNot specified717 cases in Turkey in 2007 108, 110
Albania (4th)
Bulgaria (4th)
Greece (2nd)
Turkey (3rd)
Russia (3rd)
Toscana virus infectionItaly (2nd)Not specified30–80% of meningitis cases in some areas of Italy [111]
France (2nd)
Spain (2nd)
Cyprus (2nd)
Greece (2nd)
Portugal (2nd)
Germany (2nd)
Tick-borne encephalitisLithuania (3rd) and elsewhere in EuropeNot specifiedNot specified 112, 113

Selected arboviral infections have also emerged in Southern Europe.104 In 2007, chikungunya virus infection, transmitted by Aedes mosquitoes, emerged in Italy after a man visiting from India developed symptoms.106 The outbreak was believed to have occurred following the re-emergence of chikungunya virus infection on the Indian subcontinent.107 Other arboviral infections, not necessarily considered as neglected tropical diseases, have also emerged, including West Nile fever virus in Romania, Bulgaria, Italy, and France,108 and Crimean-Congo hemorrhagic fever, a bunyavirus infection, which has emerged in Southeastern Europe and Russia,108, 109 with the number of cases rising each year in Turkey since 2002.110 Toscana virus infection (sandfly fever) is now considered an important cause of aseptic meningitis during the summer months in Italy and other Mediterranean countries.111 Over the last 30 years tick-borne encephalitis has emerged in Europe,112 and it is an important cause of neurologic disease in Lithuania.113 Arbo-Zoonet (an EU-based international network) was recently established in order to monitor and control these emerging viral vector-borne diseases.108 As noted above, hepatitis viruses are common among the Roma,114 with high rates of hepatitis A in the Czech Republic.115 Fewer than five cases of human rabies occur annually in Europe, with the major indigenous animal reservoirs including dogs in Eastern Europe and on the borders with the Middle East, foxes in Central and Eastern Europe, raccoons in northeastern Europe, and bats throughout the continent.116

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4. Discussion 

The neglected infections of poverty occur in two major geographic regions. In Eastern Europe, but especially in the Balkans and elsewhere in Southeastern Europe where the economy has been ravaged by war and a recent economic downturn, in selected former Soviet bloc countries not yet fully recovered from the fall of Communism, and in Turkey, high rates of parasitic infections are endemic. Among the soil-transmitted helminth infections in the region, ascariasis, trichuriasis, and toxocariasis have been linked to developmental and cognitive delays in childhood and reductions in childhood education and future wage-earning.1, 2 High rates of intestinal protozoan infections and congenital toxoplasmosis in Eastern Europe and Turkey would likely contribute to this problem. Also of concern are selected food-borne helminth infections in the region, including trichinellosis, opisthorchiasis, taeniasis, and cystic echinococcosis.67, 117, 118 Brucellosis and leptospirosis are two important bacterial zoonoses endemic to Eastern Europe, but especially the Balkans, and congenital syphilis has emerged as an important public health threat in the former Soviet bloc countries. Among the key policy recommendations to consider for these neglected infections of poverty are those similar to the ones recommended for similar conditions in the USA,3 including increased efforts to provide active surveillance and the urgency to determine the full extent of helminth infections and bacterial zoonoses in Eastern Europe in terms of prevalence, incidence, geographic distribution, disease burden, and adverse economic impact. There is also an urgent need to determine the ecological factors and mechanisms that account for transmission of these diseases within European borders. Pozio118 has also provided key recommendations for public health interventions against the major helminthic and bacterial zoonoses in Europe, including increased education for consumers, farmers and shepherds, improvements in farming conditions, control of sewage on pastures and drinking water, and reductions in contacts between livestock and wild animals. Newborn screening for toxoplasmosis is also critical for determining the full extent of this condition in Eastern Europe and for identifying infants at risk who might benefit from anti-protozoan chemotherapy.

A second important focus of neglected infections is in Southern Europe where vector-borne zoonoses has emerged. These infections include high rates of leishmaniasis or Chagas disease in Spain, France, Italy, and Greece, and key arboviral infections such as chikungunya, Crimean-Congo hemorrhagic fever, and Toscana virus infections in Italy and throughout Southern Europe. Critical to the success of public health control measures against such vector-borne infections are the establishment of the European Centers for Disease Control and Prevention (ECDC), founded in 2003 in order to prevent communicable disease transmission in Europe,119 and Arbo-Zoonet, which was specifically established for the control of emerging viral vector-borne diseases.108 Selected helminthiases also occur in Southern Europe including echinococcosis, fascioliasis, and strongyloidiasis. Expanded efforts to provide active surveillance and conduct disease transmission studies are warranted there as they are for Eastern Europe. Investigators from the ECDC have identified risk factors for infectious disease inequalities and possible interventions and policy directives,119 which include the policy recommendations outlined above. Such recommendations would apply to the major neglected infections of poverty in both Eastern and Southern Europe, as well as to three major vulnerable populations – the Roma, immigrants from low- and middle-income countries, and orphans destined for international adoption.

Additional opportunities exist for international cooperation. The USA and Europe share several neglected infections of poverty in common, including the helminth infections, especially ascariasis and toxocariasis, the protozoan infections Chagas disease and leishmaniasis, the bacterial infections leptospirosis and congenital syphilis, and some of the arboviral infections.6 These same infections are also endemic to sub-Saharan Africa or Latin America. Together with the USA and Europe, the suggestion has been made that all of these regions share a common history thereby providing a rationale for tackling them within an ‘Atlantic world’ framework.6 There is precedent for the USA and Europe cooperating on neglected disease studies. For example, zoonotic infections were extensively studied during a 37-year Polish and American collaboration,65 which included close and long-term cooperation with veterinary scientific institutions.117 Within this context, a possible role for the North Atlantic Treaty Organization (NATO) could be considered for international neglected disease control. Established originally as a military alliance to cement ties between the USA and Europe and to prevent Soviet domination in the North Atlantic, NATO is in search of a new mission and purpose since the fall of communism.120, 121 Increasingly, NATO could participate in a new peacetime role in the North Atlantic that could include an assault on neglected infections. With this in mind, during the 1990s President Clinton established a Partnership for Peace, which included the NATO countries together with the successor states of the former Soviet Union and its former Eastern European satellites.120 An important activity of a re-purposed NATO or Partnership for Peace could include neglected infection control in the context of medical diplomacy, referring to disease control efforts to promote nation building.6, 122, 123

Finally, efforts are needed to increase research and development efforts for Europe's neglected infections. Better diagnostic methods are needed to detect these infections in humans and to detect parasites and bacteria in slaughtered animals and in foods.118 New control tools are also required, including animal vaccines to interrupt the transmission of zoonoses to humans,124 and human vaccines for many of the helminth infections, and the bacterial zoonoses and arboviral infections described here.125 A scientific and public health assault on Europe's neglected infections of poverty that includes increased surveillance, epidemiological transmission studies, research and development for new control tools, and a policy framework, would represent a comprehensive effort to eliminate some that continent's most glaring health disparities. Increased recognition of some neglected infections in non-endemic areas like Europe, may also have a positive effect on increasing recognition of these diseases and lead to opportunities for research and testing control measures in countries where patients are not ordinarily re-infected.26

Conflict of interest: PJH is a co-founder of the Global Network for Neglected Tropical Diseases. He is an inventor on US Patent 7,303,752 B2 (issued December 4, 2007) entitled “Hookworm vaccine”. MG has no conflicts. No funds were received for this work.

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PII: S1201-9712(11)00117-2

doi:10.1016/j.ijid.2011.05.006

International Journal of Infectious Diseases
Volume 15, Issue 9 , Pages e611-e619, September 2011