Similar to 2020, the COVID-19 pandemic has meant that both antibiotic sales and the number of cases of notifiable antibiotic-resistance bacteria in humans have been lower than usual. Fewer cases of most communicable diseases in humans have been reported during the pandemic, including cases of notifiable antibiotic resistance. For notifiable infections, the difference from before the pandemic was smaller in 2021 than in 2020, while MRSA and ESBL continued to decrease in 2021. Resistance levels among clinical isolates from humans, however, were relatively unaffected by the COVID-19 pandemic. The COVID-19 pandemic has had an extensive impact on society and healthcare and has also affected the sampling for bacteriological culture, the number of health care visits, and the nature of the visits within healthcare in general.
The situation in Sweden regarding antibiotic resistance in bacteria from humans has been, and still is, favourable from an international perspective. One contributing factor is that our strategies to promote the responsible use of antibiotics and to limit the spread of antibiotic resistance are effective. Despite our relatively good situation, there are problems with cross infection and increasing antibiotic resistance, which calls for continued efforts in preventive work. Important examples are the recurrent outbreaks of vancomycin-resistant enterococci in hospitals, and an increasing number of health care related clusters of ESBLCARBA.
Antibiotic sales for humans continued to decrease in 2021, after a considerable reduction in 2020.
During the past decades, consumption of broadspectrum antibiotics has shifted towards narrow-spectrum antibiotics. However, this development seems to have gradually reversed in the recent years. In veterinary medicine, sales of antibiotics have decreased markedly since the mid-1980s, and in recent years sales seem to have stabilised at a comparatively low level. The occurrence of resistance among bacteria from animals has generally been stable at low or moderate levels. For some substances and in some bacteria the occurrence of resistance is even declining. One example of this is a significant decline of the occurrence of ESBL-producing Escherichia coli among broilers. There are however exceptions, and for example resistance to ampicillin, sulphonamides, and trimethoprim has increased in indicator E. coli from both broilers and pigs.
Key findings 2021
- Total sales of antibiotics for humans in Sweden decreased by 3% in 2021 compared to 2020, as measured in DDD per 1 000 inhabitants per day. The decrease was reflected in both outpatient and inpatient care, with the exception of acute care hospitals where antibiotic sales increased considerably. Antibiotic sales in dentistry increased with 3% in 2021.
- Antibiotic sales in outpatient care increased between the second and fourth quarter of 2021 compared to the same time period in 2020. In particular, sales of antibiotics commonly used for respiratory tract infections in children contributed to this increase.
- The proportion of MRSA among Staphylococcus aureus isolated from blood has decreased to 2.0%, compared to 2.3% in 2020.
- No new clusters of health care related ESBLCARBA were reported in 2021.
- During the pandemic, the number of cases has decreased for most types of notifiable antibiotic resistance. However, this effect is not seen in resistance levels among clinical isolates from humans, which are relatively unaffected.
- Sales of antibiotics for animals are stable at a low level and are dominated by narrow-spectrum penicillin.
- MRSA is uncommon among both farm and companion animals.
- ESBL-producing E. coli is generally uncommon among farm and companion animals as well as on meat. However, using selective methods, such bacteria could be isolated from 12% of caecal samples from bovines under one of age. The number of samples is, however, limited.
- ESBLCARBA-producing bacteria have not been confirmed in domestic animals in Sweden.
Sales of antibiotics
Sales of antibiotics for humans
The total sales of antibiotics for humans in Sweden were 3% lower in 2021 and were estimated at 9.7 DDD per 1 000 inhabitants per day. This figure encompasses all antibiotics sold on prescription to individuals and all antibiotics sold to hospitals and other health- and social care facilities.
Outpatient care
In 2021, 230 prescriptions per 1 000 inhabitants were dispensed at pharmacies in Sweden, a decrease of 3% compared to 2020. Among the 21 regions in Sweden, 19 regions achieved the national long-term target of 250 or fewer prescriptions per 1 000 inhabitants and year. Antibiotic sales decreased in all age groups with the exception of children aged 0-4 years, where sales increased by 11.4% compared to the year before. The most substantial increase occurred during the fourth quarter of 2021, where sales of antibiotics to children increased by 143% compared to the same time period in 2020. This increase consisted primarily of antibiotics commonly used against respiratory tract infections. The sales of antibiotics in dentistry increased by 3% in 2021, and accounted for 7% of all antibiotic prescriptions during the year. Since 2007, antibiotics prescribed by dentists have decreased by half.
Hospitals and other health and social care facilities
In 2021, the sales of antibiotics on requisition decreased with 5% to 1.3 DDD per 1 000 inhabitants per day. This includes all antibiotics sold to hospitals and other health- and social care facilities. Antibiotic sales to acute care hospitals increased during 2021, as measured both in DDD per 100 admissions and per 100 patient days, and reached its highest values in a five-year period. In particular, sales of broad-spectrum antibiotics increased, whereas sales of beta-lactamase-sensitive penicillins and macrolides decreased. Large regional variations were observed in the use of broadspectrum antibiotics, which is consistent with previous years.
Sales of antibiotics for animals
In 2021, reported sales of antibiotics for animals were 9 129 kg, of which 57% were narrow-spectrum penicillins. The corresponding figures for 2012 were 11 385 kg and 53%, respectively. Sales of antibiotics that should be used with special restrictions (fluoroquinolones, third generation cephalosporins and polymyxins) have decreased considerably since 2012 (by 84-95%). During the past decade, the proportion of products for the treatment of individual animals has been over 90% of the total sales. Since the withdrawal of growth-promoting antibiotics from the Swedish market in 1986, the total sales of antibiotics corrected for population sizes over time have decreased by more than two thirds. During the 1990s, sales of veterinary products for medication of groups of animals decreased, and in the past decade there has also been a decrease in sales of products for use in individual animals.
Comparing sales of antibiotics in human and veterinary medicine
In 2020, a total of 53.3 tonnes of antibiotics were sold for human use and 9.0 tonnes were sold for animal use (excluding products for intramammary or intrauterine use). Measured as milligrams of active substance per kilogram biomass, the sales were 79.3 and 11.8 milligrams per kilogram, respectively. Antibiotic sales for humans still dominate for all included classes of antibiotics except for aminoglycosides.
Notifiable resistance
ESBL-producing Enterobacterales (previously Enterobacteriaceae)
ESBL-producing Enterobacterales (previously Enterobacteriaceae) in humans has been subject to mandatory notification since 2007. It is the most common type of notifiable antibiotic resistance.
Results 2021, Enterobacterales (previously Enterobacteriaceae) with ESBL
- Number of reported cases: 7 860 (previous year 8 230), relative change –4%.
- Number of bloodstream infections: 719 (previous year 727).
- As in previous years, Escherichia coli was the most common species, (85%), followed by Klebsiella pneumoniae, (9%).
- The proportion of E. coli from blood cultures that are resistant to third-generation cephalosporins has decreased to 7%, from 8% in 2020.
- Escherichia coli was the most common species, (87%), followed by Klebsiella pneumoniae, (9%).
Results 2021, Enterobacteriaceae with ESBLCARBA
- Number of reported cases: 137 (previous year 128), relative change +7%.
- Number of bloodstream infections: 7 (previous year 11).
- Among Enterobacterales (previously Enterobacteriaceae) with ESBLCARBA, E. coli was the most common species, (58%) followed by Klebsiella pneumoniae (31%). The proportion of E. coli from blood cultures resistant to meropenem was 0.1%, compared to 0% in 2020.
ESBL-producing Enterobacterales (previously Enterobacteriaceae) are generally rare among animals in Sweden. Previously, the occurrence in intestinal samples from broilers was high but it has decreased in recent years. In 2021, the occurrence of ESBL-producing E. coli in intestinal samples from pigs, cattle under one year, and broilers, as well as samples of pig and bovine meat was investigated with selective methods. Such bacteria were isolated from 1% of the intestinal samples from pigs, 12% of the intestinal samples from cattle under one year, and 1% of the intestinal samples from broilers. The number of samples from cattle under one year is however limited. Furthermore, such bacteria were isolated from <1% and 0% of bovine and pig meat of Swedish origin.
ESBLCARBA-producing bacteria has not been confirmed in domestic animals in Sweden.
Methicillin-resistant Staphylococcus aureus (MRSA)
Community-acquired infection has long been the most common type in humans, accounting for half of the cases. In 2015, community-acquired infection was divided into family/household-related infection and community-acquired infection. Family/household-related infections and communityacquired infections accounted for 33% and 16% of the cases, respectively.
Results 2021
- Number of reported cases: 2 895 (previous year 3 112), relative change -7%.
- Number of bloodstream infections: 97 (previous year 98).
- The proportion of MRSA among Staphylococcus aureus isolated from blood has decreased to 2.0%, compared to 2.3% in 2020.
The occurrence of MRSA in animals in Sweden is still low, which limits the spread from animals to humans. MRSA was found sporadically in horses, dogs and cats. In horses the number of MRSA cases in 2021 (n=23) was, as in 2020 (n=27) higher than in previous years. The previous highest figure was in 2014 (n=9). The increase could partly be explained by an outbreak in an equine hospital with eight cases. The outbreak in horses was caused by a, for horses in Sweden new spa-type, t034, belonging to the livestock-associated MRSA clonal complex 398. In companion animals, the same types of MRSA as in humans dominate, indicating a human source of MRSA in these animals.
Methicillin-resistant Staphylococcus pseudintermedius (MRSP)
In 2021, the number of reported cases of methicillin-resistant Staphylococcus pseudintermedius (MRSP) in animals was around the same level as in previous years. In total 43 cases of MRSP were notified to the Swedish Board of Agriculture, including 41 from dogs, one from a cat and one from a horse. All isolates were available for further investigations. When MRSP first occurred among animals in Sweden, the sequence type ST71 dominated. However, for several years the isolates of MRSP have been more diverse with several sequence types occurring.
MRSP in humans is not notifiable.
Streptococcus pneumoniae with reduced susceptibility to penicillin (PNSP)
Results 2021
- Number of reported cases: 92 (previous year 112), relative change –17%.
- Number of bloodstream infections: 3 (previous year 4).
- The proportion of S. pneumoniae with reduced susceptibility to penicillin (PNSP) among bloodstream infections decreased to 6.3% from 8.3% 2020.
Vancomycin-resistant enterococci (VRE)
Results 2021
- Total number of reported cases: 209 (previous year: 79), relative change +64%.
- The number of cases of VRE can vary greatly between years depending on the number and magnitude of hospital outbreaks.
- Number of reported cases of E. faecium with vancomycin resistance: 204 (previous year: 77), relative change +65%
- Number of reported cases of E- faecalis with vancomycin resistance: 1 (previous year: 4)
- There were three cases infected with both E. faecium and E. faecalis.
• Number of bloodstream infections: 2 (previous year: 4) - Eleven clusters were reported during the year with 2-36 cases each. Out of these, five were large hospital-related outbreaks with 11-36 cases each. In 2020, eight hospitalrelated outbreaks were reported.
- The proportion of VRE among bloodstream infections is low at, 0.3% for E. faecium resistant to vancomycin and 0.1% for E. faecalis resistant to vancomycin.
Zoonotic pathogens
Salmonella is rare in animals in Sweden. Furthermore, only a few of the notified cases involve antibiotic-resistant strains. Resistance to fluoroquinolones is rare. For Salmonella species isolated from human faeces, the highest occurrence of resistance was to fluoroquinolones, (17%). No resistance to meropenem was reported. Isolates from human invasive infections with Salmonella are markedly more resistant, probably due to the large proportion of cases acquired abroad.
Campylobacter from animals in Sweden are generally susceptible to relevant antibiotics, and resistance to erythromycin, for example, is most uncommon. In Campylobacter jejuni from humans, resistance to ciprofloxacin was 45% and resistance to tetracycline was 17% 2021, and 1% were resistant to erythromycin.
Infections, either in humans or in animals, caused by Salmonella and Campylobacter are usually not treated with antibiotics. In humans, only a small proportion of the isolates, most of which are related to serious infections, are tested for antibiotic susceptibility.
Human clinical isolates
All data for these compilations are collected automatically via Svebar, a collaboration between the clinical microbiology laboratories and the Public Health Agency.
- Escherichia coli: Resistance in blood isolates to ceftazidime and cefotaxime was 6-7%. The number of reported E. coli ESBL from blood was 575 cases in 2021. Resistance to ciprofloxacin is now 14% and 10%, respectively, in isolates from blood and urine. This needs to be considered when choosing empirical treatment for febrile urinary tract infection.
- When E. coli from urine are divided by age and gender, some differences in resistance are seen. Most prominent is the high ciprofloxacin resistance (17-19%) seen among men 20 years and older.
- Klebsiella pneumoniae: resistance in blood isolates to cefotaxime and ceftazidime was 6-7%. The number of reported K. pneumoniae ESBL from blood was 97 cases in 2021. As for E. coli, resistance to ciprofloxacin is now relatively high at, 8-11% in isolates from urine and blood.
- Staphylococcus aureus: Resistance to cefoxitin (which is indicative of MRSA) in isolates from blood and samples from skin and soft tissue was 2.0% and 1.9% respectively. The number of reported MRSA from blood was 97 cases in 2021.
- Enterococcus faecalis and Enterococcus faecium: Vancomycin resistance in isolates from blood remains low (0.1% and 0.3%, respectively) and the high-level aminoglycoside resistance has gradually decreased since 2017.
- Clostridioides difficile: The incidence is now 61 cases per 100 000 inhabitants and has remained rather stable since 2018. No isolates were tested for antibiotic resistance in 2021.
Animal clinical isolates
Bacteria causing clinical disease in animals are mostly susceptible to antibiotics relevant for treatment. Respiratory pathogens from farm animals and horses are generally susceptible to benzylpenicillin, but penicillin resistance is common in Staphylococcus pseudintermedius from dogs and occurs in S. aureus from horses and S. felis from cats. However, in S. schleiferi from dogs penicillin resistance is uncommon. Resistance to commonly used antibiotics in E. coli occurs in all animals but is most prominent in enteric isolates from young calves and pigs. Susceptibility testing for guidance in antibiotic therapy is warranted, especially for staphylococci, E. coli, and Brachyspira spp.
Indicator bacteria from healthy animals
Antibiotic resistance in E. coli from the intestinal flora of healthy animals serves as an indicator for the presence of resistance in an animal population. The prevalence of acquired resistance in such commensal bacteria also indirectly indicates the magnitude of the selective pressure from the use of antibiotics in an animal population. The prevalence of resistance in indicator bacteria from animals in Sweden is low, and the situation is favourable in an international perspective. As an example, in the latest investigations of indicator E. coli from broilers and pigs, 72% and 64% respectively, were susceptible to all tested substances.