During January 1, 2000–December 31, 2009, a total of 295 infections caused by spore-forming bacteria (157 botulism, 33 tetanus, 92 C. novyi, and 13 anthrax) were reported among PWID in England and Scotland; the overall infection rate was 1.83 cases per 1,000 PWID. Two thirds (199) of these cases were reported in England and one third (96) in Scotland, corresponding to rates of 1.45 and 4.01 per 1,000 PWID, respectively (Table 1).

The number of reported cases varied over time (Figure 1). The C. noyvi infections and anthrax cases were clustered in 2000 and 2009, respectively, and most tetanus cases occurred during 2003–2005. By contrast, botulism was reported in all years; the annual number of cases varied from 3 to 41.

Infection rates varied by health region. In England, rate of infection varied from 0.68 cases per 1,000 PWID for the West Midlands to 2.02 for the East of England (Figure 2); rates were also high for the East Midlands, London, and the North West (1.7, 1.9, and 1.7 cases/1,000 PWID, respectively). In Scotland, rates ranged from zero in 3 rural areas with small populations of PWID (Ayrshire and Arran, Borders, and Highlands) to 7.7 per 1,000 PWID in Greater Glasgow and Clyde; rates were also high in Grampian (3.6 cases/1,000 PWID) and Fife (3.9 cases per /1,000 PWID).

In terms of specific infections, the rate of botulism was slightly higher for England than for Scotland, although this difference was not statistically significant (1.0 vs. 0.8 cases/1,000 PWID, p = 0.232), and rates of tetanus were similar for both countries (0.20 vs. 0.21/1,000 PWID, p = 0.962). In contrast, rates of C. novyi infections and anthrax were markedly higher for Scotland than for England (2.5 vs. 0.2 cases/1,000 PWID, p<0.001; and 0.5 vs. 0 cases/1,000 PWID, p<0.001, respectively). C. novyi infections were particularly concentrated in Greater Glasgow and Clyde (5.6 cases/1,000 PWID) and in the North West region of England (0.7 cases/1,000 PWID). Higher than average rates of botulism were reported in the East of England region (1.8 cases/1,000 PWID) and in Grampian (2.0 cases/1,000 PWID).

When we compared the demographic characteristics of case-patients with those of PWID participating in the 2 national surveys, we found that the proportion of female patients with tetanus, C. novyi infection, and anthrax was higher (38%–60%) than the proportion of female PWID in the community (24%–26%) (Table 2). These differences were statistically significant for C. novyi infections in England and Scotland (p = 0.011 and p<0.001, respectively) and for tetanus cases in England. In England, the median age of PWID with botulism, tetanus, and C. novyi infection ranged from 33 to 37 years; this age range was higher among those with botulism than among the PWID participating in the Unlinked Anonymous Monitoring Survey (37 vs. 32 years; p<0.001). In Scotland, the median ages of PWID with botulism, C. novyi infection, and anthrax were comparable to the median age of PWID from the community sample; whereas, the median age was higher for PWID infected with tetanus (47 vs. 33 years), although not significantly so (p = 0.065).

Of the 295 reported case-patients, 52 (18%) are known to have died. Of these, 8 (5%) died of botulism, 2 (6%) died of tetanus, 36 (39%) died of C. novyi infection, and 6 (46%) died of anthrax.

Over the decade beginning in 2000, almost 300 severe infections caused by spore-forming bacteria were reported among PWID in England and Scotland; 52 of these patients died. The distribution of the cases varied markedly between these countries. In Scotland, the number of cases was excessive relative to the estimated population of PWID when compared with England; this excess, however, is mainly attributable to an excess of C. novyi infections and anthrax cases. In contrast, rates of botulism and tetanus for Scotland were lower than and comparable with, respectively, those for England.

In the United Kingdom, microbiological testing has usually been unable to confirm the presence of these bacterial species in seized or surrendered heroin (2), although, in 2009, C. botulinum was isolated from 1 sample of heroin seized in Scotland (K.A. Grant, pers. comm.). Nevertheless, it is generally recognized that the infections discussed here have resulted from contaminated heroin, which might have become contaminated during processing, transport, or storage. In the United Kingdom, 90% of heroin used originates in Afghanistan, where the opium is produced and—increasingly since 2002—converted to heroin. Heroin from Afghanistan usually travels over land, passing through several countries before entering the European Union and reaching the United Kingdom (17,18). The conditions in which heroin is processed, transported, and stored are uncertain; because these activities are illegal, they all probably make the drug vulnerable to inadvertent contamination with bacterial spores, for example, from soil or dust. Contaminated heroin is thought to have been the source of B. anthracis infection in a drug injector in Norway in 2000 (19,20) and in the more recent outbreak among PWID in Europe (12). Another source of potential contamination is drug adulterants (cutting agents), which are widely used to dilute and increase the bulk of illicit drugs (21). Although most infections probably resulted from upstream (before it reaches the end user) contamination of heroin, spores on the soiled hands of users and dirty needles could be inoculated during the injection process (22). This mode of infection remains unproven, although signs of tetanus were observed by Arthur Nicolaier in 1884 after he injected garden soil containing C. tetani (at that point unnamed) into animals (23), and clostridial infections after injection through dirt-covered hides have been reported (24).

Although the presence of bacterial spores is a necessary prerequisite for infection, several other factors might influence the development and geographic patterns of infections. The clustering of cases of C. novyi infection; anthrax; and, to a lesser extent, tetanus into outbreaks suggests that the contamination might have affected specific batches of heroin. By contrast, the botulism cases were generally more sporadic (albeit with some clustering) (25,26), suggesting that C. botulinum and, to a lesser degree, C. tetani spores might be more commonly present in the drug supply or in the local environment but at varying levels of contamination. Different drug supply routes serving eastern and western England and Scotland (12) might account for some of the geographic patterns and are consistent with the excessive C. novyi infections among PWID in Greater Glasgow and Clyde (western Scotland) and the North West region of England and with the higher rates of botulism among PWID in the East of England and Grampian (eastern Scotland).

Practices such as skin or muscle popping (intentionally or accidentally injecting into skin or muscle) (10,27,28) or the use of large amounts of citric acid to dissolve heroin can damage soft tissue, leading to necrosis and providing a suitable environment for anaerobic bacteria, such as Clostridium spp., to thrive. Older age (a proxy for a longer injecting career) and female sex have been associated with infections and injuries at injecting sites (29,30), which are associated with difficulty accessing veins. These persons might resort to injecting into the skin or muscle. Geographic variation in these practices might explain some of the variations seen in this study. PWID across England and Scotland might be regularly exposed to botulism and tetanus spores, but the levels of infection might be higher in some areas where skin or muscle popping is more common. This finding is consistent with the high proportion of women and the older median age among PWID with clostridial or B. anthracis infections described here in comparison with the wider population of PWID in England and Scotland. The emergence of these infections as a major public health issue in the United Kingdom and Ireland (6) over the past decade might reflect the changing characteristics of the drug-using population, an aging cohort of users resulting from the marked increase in injection drug use during the 1980s and 1990s (31). With regard to tetanus, variation could also reflect differences in the levels of effective immunization among PWID.

This analysis captures only the anthrax cases reported before the end of December 2009; however, the anthrax outbreak continued into 2010 and resulted in a total of 52 confirmed cases, including 5 in England (12,32). The risk factors for anthrax might differ from those for the other infections/diseases because anthrax is the only disease considered here that is caused by an aerobic bacterium. Furthermore, we cannot exclude the possibility of inhalational anthrax in some of the case-patients who reported smoking heroin (11,12). We considered only confirmed cases of anthrax in this analysis; however, the inclusion of probable cases (although it would have increased the numbers and rates) most likely would not have changed our findings with regard to demographic characteristics, given that probable and confirmed cases were similar in terms of age (mean 34 vs. 35 years, respectively) and sex (29% vs. 30% female, respectively) (12).

Because infections might go unreported or be misdiagnosed, the data presented here potentially underestimate the actual numbers of infections among PWID in England and Scotland. For tetanus and botulism, little toxin is required to cause symptoms; therefore, in combination with a reported history of injection drug use, index of clinical suspicion should be high (33–35). However, tetanus cases are underreported because some clinicians are not familiar with this rare disease (36). Misdiagnosis of infection might also account for underreporting because the symptoms of other illnesses can resemble those of the infections of interest in this study (e.g., Guillain-Barré syndrome vs. botulism) (33,34). In addition, if an injection site infection is treated promptly with broad spectrum antimicrobial drugs before tissue samples are collected, microbiological confirmation might not be possible (7).

Another limitation of this study is associated with estimates of the size of the PWID population. The estimates from Scotland and England were produced by using indirect methods by the same team but were based on different data sources and definitions. Moreover, estimates produced by indirect methods are difficult to validate. For example, the national study used here estimated 17,909 PWID in London (13), but another study estimated >30,000 PWID in London for 2000–2001 (37).

Because the quality and safety of illicit heroin is not monitored or controlled, sporadic cases and outbreaks of illness associated with spore-forming bacteria among PWID might continue. Persons who use heroin should be encouraged to seek treatment for their dependency. Health care professionals should educate PWID who continue to inject about injecting hygiene, the risks from specific injecting practices that have been associated with these infections, the need to ensure that their tetanus vaccinations are up to date, and the need to seek care if they have symptoms of an injection-related infection. Public health professionals should continue to be vigilant to ensure prompt detection of outbreaks and so permit the rapid dissemination of advice.