Abstract
The recent anthrax outbreak among injecting drug users (IDUs) in Europe has highlighted an ongoing problem with severe illness resulting from spore-forming bacteria in IDUs. We collated the numbers of cases of 4 bacterial illnesses (botulism, tetanus, Clostridium novyi, and anthrax) in European IDUs for 2000 to 2009 and calculated population rates. Six countries reported 367 cases; rates varied from 0.03 to 7.54 per million people. Most cases (92%) were reported from 3 neighboring countries: Ireland, Norway, and the United Kingdom. This geographic variation needs investigation.
The emergence of anthrax among injecting drug users (IDUs), mostly of heroin, in Scotland in 20091 constituted the second major cluster of severe bacterial illness among IDUs in the country in a decade. In 2000 and 2001, an outbreak of Clostridium novyi affected IDUs across Great Britain and Ireland,2,3 with the majority of cases observed in Scotland. Since then, there have been ongoing reports of illness and death among IDUs taking heroin in the United Kingdom. These cases have been associated with a range of spore-forming bacteria, with wound botulism and tetanus cases continuing to occur since being first reported in the early 2000s.4–6 Contaminated heroin, mainly supplied to the United Kingdom and other European countries via trafficking routes emanating from Afghanistan,7,8 is considered to be the likely source of infection in most, if not all, instances. However, the basic geographic epidemiology of these infections among IDUs in Europe has not been described. To ascertain whether what is being observed in the United Kingdom is unique or is similar to what is occurring elsewhere in Europe, we explored differences in rates of severe infections among IDUs caused by 4 spore-forming bacteria that have been associated with contaminated heroin. Such analysis might provide insights into where, for example, contamination of heroin is occurring.
METHODS
We collated reports of clinically or microbiologically confirmed infections caused by Clostridium botulinum (botulism), Clostridium tetani (tetanus), C. novyi, and Bacillus anthracis (anthrax) among IDUs in Europe. For the United Kingdom, we extracted cases with dates of onset between January 2000 and December 2009 from national surveillance systems operated by Health Protection Agency and Health Protection Scotland.5 Through searches of PubMed and European public health journals, we identified published reports of cases in other European countries during the 10-year period. We then consulted the European Monitoring Centre for Drugs and Drug Addiction (EMCDDA)9 network of infectious disease experts10,11 to identify further published and unpublished reports. Of the 28 EMCDDA member countries (excluding the United Kingdom) contacted, all responded. There are problems with the comparability of available estimates of number of IDUs in each country; therefore, we used both available IDU estimates and 2005 population data to calculate rates.
RESULTS
We identified 367 infections over the 10-year period. Of these cases, 300 occurred in the United Kingdom; 160 were caused by C. botulinum, 34 by C. tetani, 93 by C. novyi, and 13 by B. anthracis, giving an overall rate of 5 infections per million people and 1.9 to 2.1 infections per 1000 IDUs (Table 1). Six other European countries (Germany, Greece, Ireland, Italy, Netherlands, and Norway) reported cases since 2000: 39 caused by C. botulinum, 3 by C. tetani, 23 by C. novyi, and 2 by B. anthracis (Table 1). Rates of infection with spore-forming bacteria among IDUs in these countries were much lower than were those in the United Kingdom (Table 1), except in Ireland (7.54 infections/million, 3.9–6.6 infections/1000 IDUs). Norway was the only other country to report more than 1 infection per million.
TABLE 1—
Country | Population in 2005 | Estimated IDUs |
Bacterial Infections |
Summary of Responses to Request for Further Information on IDU Cases | References | |||||||||
Range | Central Estimate, No. | Year | Method | Botulism, No. | Tetanus, No. | Clostridium noyvi, No. | Anthrax, No. | Total No. | Rate/ Million People | Rate/ 1000 IDUs | ||||
Austria | 8 206 524 | 12 000–23 000 | NA | 2000 | MM | 0 | 0 | 0 | No cases reporteda | |||||
Belgium | 10 445 852 | 23 200–28 400 | NA | 1997 | HM | 0 | 0 | 0 | No cases reportedb | |||||
Bulgaria | 7 761 049 | No data on injecting status | ||||||||||||
Croatia | 4 443 901 | 2521–4167 | 3145 | 2009 | MM | 0 | 0 | 0 | No cases reported | |||||
Cyprus | 749 175 | 379–646 | 481 | 2009 | OT | 0 | 0 | 0 | No cases reported | |||||
Czech Republic | 10 220 577 | 34 200–36 400 | 35 300 | 2009 | TM | 0 | 0 | 0 | No cases reported | |||||
Denmark | 5 411 405 | 10 066–16 821 | 12 754 | 2006 | CR | 0 | 0 | 0 | No cases reported | |||||
Estonia | 1 347 510 | 8132–34 443 | 13 886 | 2004 | CR | 0 | 0 | 0 | No cases reported | |||||
Finland | 5 236 611 | 12 200–19 700 | 15 650 | 2002 | OT | 0 | 0 | 0 | No cases reported | |||||
France | 62 637 596 | NA | 122 000 | 1999 | HM | 0 | 0 | 0 | No cases reported | |||||
Germany | 82 500 849 | 78 000–110 500 | NA | 2005 | MM | 21 | 1 | 22 | 0.27 | 0.20–0.28 | Botulism: 4 more cases | 12–17 | ||
Greece | 11 082 751 | 8999–12 713 | 10 658 | 2009 | CR | 1 | 2 | 3 | 0.27 | 0.24–0.33 | Botulism: 1 case; tetanus: 2 casesc | |||
Hungary | 10 097 549 | NA | 5699 | 2008–2009 | OT | 0 | 0 | 0 | No cases reportedd | |||||
Ireland | 4 109 173 | 4694–7884 | NA | 1996 | MM | 9 | 22 | 31 | 7.54 | 3.9–6.6 | No additional cases | 18–20 | ||
Italy | 58 462 375 | NA | 326 000 | 1996 | HM | 2 | 2 | 0.03 | 0.0061 | Botulism: 2 cases | ||||
Latvia | 2 306 434 | 0 | 0 | No cases reported | ||||||||||
Lithuania | 3 425 324 | 0 | 0 | No cases reportede | ||||||||||
Luxembourg | 461 230 | 1253–1919 | 1485 | 2007 | OT | Unable to provide data | ||||||||
Malta | 402 668 | 0 | 0 | No cases reported | ||||||||||
The Netherlands | 16 305 526 | 2336–2444 | 2390 | 2008 | TM | 1 | 1 | 2 | 0.12 | 0.82–0.86 | No additional cases | 21,22 | ||
Norway | 4 606 363 | 8 810–12 480 | 10 238 | 2008 | MM | 5 | 1 | 1 | 7 | 1.52 | 0.56–0.79 | Botulism: 4 more cases | 23 | |
Poland | 38 173 835 | 0 | 0 | No cases reportedf | ||||||||||
Portugal | 10 529 255 | 13 183–16 285 | NA | 2005 | TM | 0 | 0 | 0 | No cases reported | |||||
Romania | 21 658 528 | 0 | 0 | No cases reported | ||||||||||
Slovakia | 5 384 822 | 13 732–34 343 | 18 841 | 2006 | TM | 0 | 0 | 0 | No cases reported | |||||
Slovenia | 1 997 590 | NA | 7320 | 2001 | OT | 0 | 0 | 0 | No cases reported | |||||
Spain | 43 038 035 | NA | 83 972g | 1998 | MM | 0 | 0 | 0 | No cases reported | |||||
Sweden | 9 011 392 | 0 | 0 | No cases reported | ||||||||||
United Kingdom | 60 059 900 | 143 298–156 017 | 147 900 | 2006–2007 | OT | 160 | 34 | 93 | 13 | 300 | 5.00 | 1.9–2.1 | Not applicable | |
Totalh | 491 851 520 | 199 | 37 | 116 | 15 | 367 | 0.75 | |||||||
Totalh (excluding UK) | 431 791 620 | 39 | 3 | 23 | 2 | 67 | 0.16 |
Note. CR = capture recapture; EMCDDA = European Monitoring Centre for Drugs and Drug Addiction; HM = HIV multiplier; IDU = injecting drug user; MM = mortality multiplier; NA = not available; OT = other or multiple methods; TM = treatment multiplier.
Source. Estimates of numbers of IDUs are from the EMCDDA.24
No cases reported through the Austrian early warning system.
Data from 2006–2009.
Data from 2003–2009, drug user or IDU. Data on drug use not systematically collected.
Data from 2004–2009 for tetanus, and from 2006–2009 for botulism.
No information on these infections occurring among injecting drug users.
Drug use not routinely collected; however, in all known cases, other routes were implicated.
Opiate injectors only.
Excluding Bulgaria and Luxembourg.
DISCUSSION
During the period 2000 to 2009, a total of 300 severe infections caused by spore-forming bacteria among IDUs in the United Kingdom were reported. This amount is more than 4 times the number of cases—and 31 times the rate per million population—reported elsewhere in the European Union, Norway, and Croatia. The only country with a higher rate was the United Kingdom's nearest neighbor, Ireland. The country with the third highest rate, Norway, also neighbors the United Kingdom. These 3 countries accounted for 92% of the 367 cases identified, an observation indicating that these infections are concentrated in Europe's northwestern corner.
The uneven distribution of these infections may reflect underreporting; however, the reporting of anthrax, botulism, and tetanus is compulsory in all European Union countries and Norway (excepting Belgium and France, where reporting is voluntary for anthrax and botulism), which should limit underreporting,25 although a few countries reported data-quality issues (Table 1). Alternatively, variation might result from underdiagnosis of infections in some countries. However, in the context of the severe and distinct nature of the associated illnesses we believe that this is unlikely to account for such large differences. Another possible explanation could be differences in the prevalence of injecting.26 However, when we examined rates of infection using national IDU population estimates, the wide variations remained.
These infections have been postulated to arise from the environmental contamination of heroin.2,20 Accordingly, their distribution may reflect regional differences in heroin trafficking routes, heroin cutting and preparation practices, and injecting drug use practice, including the type of drug injected.26
Explaining the excess of spore-forming bacterial infections among IDUs in the northwestern corner of Europe requires further investigation, although the geographic distribution of cases suggests that contamination of heroin might occur along trafficking routes to the affected countries.7,8 The cutting of heroin with other substances is a potential source of contamination. In light of the recent anthrax outbreak1,5—during 2010, there were a further 39 cases in United Kingdom and 1 in Germany27–30—health care professionals and IDUs need to remain vigilant. Early recognition of infections arising from potentially contaminated heroin is essential so that investigations can be undertaken and appropriate public health messages disseminated. Improved surveillance of these infections among IDUs, information on bacterial genetic profiles,31,32 and the public health monitoring of illicit drug contamination33 could improve the understanding of illicit drug distribution and associated health risks.
Acknowledgments
We thank all the experts who responded to our request for further information through the EMCDDA expert network: Austria—Charlotte Wirl and Marion Weigl; Belgium—Nathalie Deprez; Bulgaria—Raina Ilieva; Croatia—Lidija Vugrinec; Cyprus—Natasa Savvopoulou; Czech Republic—Viktor Mravcik; Denmark—Kåre Mølbak; Estonia—Kuulo Kutsar; Finland—Martta Forsell; France—Marie Jauffret-Roustide and Agnes Cadet Tairou; Germany—Ruth Zimmermann; Greece—Anastasios Fotiou; Hungary—Anna Tarján; Ireland—Jean Long; Italy—Silvia Zanone; Latvia—Marcis Trapencieris; Lithuania—Vytautas Gasperas; Luxembourg—Alain Origer; Malta—Tanya Melillo Fenech; Netherlands—Esther Croes; Norway—Hans Blystad; Poland—Michal Czerwinski; Portugal—José Pádua; Romania—Andrei Botescu; Slovakia—Imrich Steliar; Slovenia—Andreja Drev; Spain—Sara Santos; and Sweden—Sofie Ivarsson.
Human Participant Protection
Protocol approval was not necessary because the data used were obtained from the outputs of public health surveillance systems and secondary sources.
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