For a long time, Sweden has had a favourable situation compared to many other countries when it comes to antibiotic resistance in bacteria from humans, which remains true. One contributing factor is that we have effective strategies to promote the responsible use of antibiotics and limit the spread of antibiotic resistance. Despite the favourable situation, there are problems with continuously increasing antibiotic resistance and the spread of infections in healthcare. Important examples are the recurrent outbreaks of vancomycin-resistant enterococci in hospitals and an increasing number of healthcare-associated clusters of ESBLCARBA. This emphasises the importance of continuous work within Strama, infection prevention and control as well as infection prevention in the community to prevent increasing antibiotic resistance.
Antibiotic sales for humans increased in 2022 after a considerable reduction in 2020 and 2021 as an effect of the COVID- 19 pandemic. In past decades, consumption has shifted from broad-spectrum antibiotics towards narrow-spectrum antibiotics. However, this development seems to have been disrupted 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 2022
- Total sales of antibiotics for humans in Sweden increased by 8.2% in 2022 compared to 2021, as measured in DDD per 1 000 inhabitants per day. The increase was reflected in both outpatient and inpatient care, as well as in acute care hospitals. Antibiotic sales in dentistry increased by 0.8% in 2022.
- Antibiotic sales in outpatient care increased during 2022 compared to 2021. Sales of antibiotics commonly used for respiratory tract infections in children during the third and fourth quarters of the year especially contributed to this increase.
- Since 2020, resistance to cefotaxime in Escherichia coli and the proportion of methicillin-resistant Staphylococcus aureus (MRSA) isolated from blood are used as indicators of antibiotic resistance in Sweden. Both the proportion of MRSA and the proportion of E. coli that are resistant to cefotaxime have slowly increased over a ten-year period to the current 1.9 and 7 percent respectively. For both indicators, the increase appears to have slowed down in recent years.
- During the pandemic, the number of cases of most types of notifiable antibiotic resistance decreased. For most of these, clear increases are now seen, most markedly for ESBL CARBA, where 240 cases were reported, compared to 137 in 2021. Resistance levels among clinical isolates from humans were not affected by the pandemic.
- An increase in resistance among Streptococcus pyogenes to clindamycin starting in the spring of 2020 has been noted, during the fall 2022 the resistance returned to previous levels, below 5%.
- One cluster of health care-related ESBL CARBA and five health care-related clusters with transmission abroad were reported in 2022.
- Eleven hospital-associated outbreaks of vancomycin-resistant enterococci were reported in 2021.
- 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.
- ESBL CARBA-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 increased by 8.2% in 2022 and was estimated at 10.2 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 2022, 251 prescriptions per 1 000 inhabitants were dispensed at pharmacies in Sweden, an increase of 9% compared to 2021. Among the 21 regions in Sweden, 10 regions achieved the national long-term target of 250 or fewer prescriptions per 1 000 inhabitants and year. Antibiotic sales increased in all age groups with the highest increase in children aged 0-4 years, where sales increased by 33.9% compared to the year before. The most substantial increase occurred during the fourth quarter of 2022. This increase consisted primarily of antibiotics commonly used to treat respiratory tract infections.
The sales of antibiotics in dentistry decreased marginally by 0.8% in 2021, and accounted for 6.6% of all antibiotic prescriptions during the year. Since 2007, the prescription of antibiotics by dentists has decreased by half.
Hospitals and other health- and social care facilities
In 2022, the sales of antibiotics on requisition, including all antibiotics sold to hospitals and other health- and social care facilities, increased. Antibiotic sales to acute care hospitals increased during 2022, as measured both in DDD per 100 admissions and per 100 patient days, reaching the highest levels observed over the last five years. In particular, sales of broad-spectrum antibiotics increased, as well as sales of betalactamase sensitive and resistant penicillins. Large regional variations were observed in the consumption of broad-spectrum antibiotics, which is consistent with previous years.
Sales of antibiotics for animals
When retrieving data for 2022, a substantial decrease compared to 2021 was noted, and a lack of completeness was suspected. Investigations to resolve the issue was initiated and a number of rejected data reports from pharmacies were identified and corrected by the pharmacies. Therefore, in this report, data since 2017 has been updated. The difference between 2021 and 2022 was still inexplicably large (-12%) and a thorough search for yet undiscovered errors was undertaken but none was identified. No explanation for this sudden decrease in sale has been identified. Hence, the results should be assessed with caution. Furthermore, if at a later stage some yet unidentified error causing a lack of completeness is discovered, data will be updated and published online on the SVA web page.
In 2022, reported sales of antibiotics for animals from pharmacies in Sweden were 8 865 kg, of which around 60% were narrow-spectrum penicillins. Sales of antibiotics that should be used with special restrictions (fluoroquinolones, third generation cephalosporins and polymyxins) have decreased considerably since 2013. 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 2022, a total of 59.3 tonnes of antibiotics were sold for human use and 8.8 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 84.6 and 11.3 milligrams per kilogram, respectively. Antibiotic sales for humans still dominate for all analysed classes of antibiotics.
Notifiable resistance
ESBL-producing Enterobacterales
ESBL-producing Enterobacterales in humans has been subject to mandatory notification since 2007. It is the most common type of notifiable antibiotic resistance.
Results 2022, Enterobacterales with ESBL
- Number of reported cases: 9 611 (previous year 7 860), relative change +22%.
- Number of bloodstream infections: 818 (previous year 719).
- As in previous years, Escherichia coli was the most common species, (82%), followed by Klebsiella pneumoniae, (10%).
- The proportion of E. coli from blood cultures that are resistant to third-generation cephalosporins were 7% as in 2021.
Results 2022, Enterobacterales with ESBL CARBA
- Number of reported cases: 240 (previous year 137), relative change +75%.
- Number of bloodstream infections: 14 (previous year 7).
- Among Enterobacterales with ESBLCARBA, E. coli was the most common species, (56%) followed by Klebsiella pneumoniae (31%).
The number of E. coli from blood cultures resistant to meropenem was 3 out of 10 541, compared to 6 out of 10 624 in 2021.
ESBL-producing Enterobacterales 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 2022, the occurrence of ESBL-producing E.coli in intestinal samples from broilers, fattening turkeys and laying hens, as well as samples of broiler and turkey meat was investigated with selective methods. Such bacteria were isolated from 2% of the intestinal samples from broilers and laying hens, respectively but not in any intestinal samples from fattening turkeys. Furthermore, such bacteria were not isolated from any of samples of turkey meat or broiler meat of Swedish origin. However, 25 % of broiler meat samples of non-Swedish origin were positive for ESBL-producing E. coli, although the number of samples are limited and hence the results should be assessed with caution.
Bacteria that produce ESBLCARBA have 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/house-hold-related infections and communityacquired infections accounted for 28% and 19% of the cases, respectively.
Results 2022
- Number of reported cases: 3 340 (previous year 2 895), relative change +15%.
- Number of bloodstream infections: 96 (previous year 97).
- The proportion of MRSA among Staphylococcus aureus isolated from blood has decreased to 1.9%, compared to 2.0% in 2021.
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, cats and one parrot. The increase of MRSA cases, compared to previous years, seen in horses in 2020 (n=27) and 2021 (n=23) was partly explained by outbreaks in equine hospitals. Consequently, in 2022 the figures dropped to 13 cases, as there were no outbreaks. 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 2022, the number of reported cases of methicillin-resistant Staphylococcus pseudintermedius (MRSP) in animals was around the same level as in previous years. In total 54 cases of MRSP were notified to the Swedish Board of Agriculture, including 52 from dogs, one from a cat and one from a orangutan. 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 2022
- Number of reported cases: 146 (previous year 92), relative
change +59%.
- Number of bloodstream infections: 9 (previous year 3).
- The proportion of S. pneumoniae with reduced susceptibility to penicillin (PNSP) among bloodstream infections
increased to 7.7% from 6.3% 2021.
Vancomycin-resistant enterococci (VRE)
Results 2022
- Total number of reported cases: 236 (previous year: 206), relative change +13%.
- 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: 227 (previous year: 204), relative change +11%
- Number of reported cases of E. faecalis with vancomycin resistance: 4 (previous year: 1)
- There were five cases infected with both E. faecium and E. faecalis.
- Number of bloodstream infections: 5 (previous year: 2)
- Sixteen clusters were reported during the year with 2-28 cases each. Out of these, six were large hospital-related outbreaks with 8-28 cases each. In 2021, eleven hospital related 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. Among 115 isolates from domestic animals in 2022 only 3 were resistant to one antibiotic each and none was resistant against fluoroquinolones.
For Salmonella species isolated from human faeces, the highest occurrence of resistance was to fluoroquinolones, (24%). No resistance to carbapenems 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 55% and resistance to tetracycline was 27% in 2022, and a half percent of the isolates 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 and 7% respectively. The number of reported E. coli ESBL from blood was 605 cases in 2022. 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 and 7% respectively. The number of reported K. pneumoniae ESBL from blood was 122 cases in 2022. As for E. coli, resistance to ciprofloxacin is now relatively high at, 10-12% 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 1.9% and 2.3% respectively. The number of reported MRSA from blood was 96 cases in 2022.
Enterococcus faecalis and Enterococcus faecium: Vancomycin resistance in isolates from blood remains low (0.1% and 0.3%, respectively) and high-level aminoglycoside resistance is still on a lower level compared to 2017.
Clostridioides difficile: The incidence has been relatively stable since 2018, but has now increased from 61 cases to 65 cases per 100 000 inhabitants and year. No isolates were tested for antibiotic resistance in 2022.
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 resistance occurs, for example in Pasteurella multocida from calves. Penicillin resistance is common in Staphylococcus pseudintermedius from dogs, Staphylococcus hyicus from pigs, 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, 69% and 64% respectively, were susceptible to all tested substances.