Global burden of Klebsiella pneumoniae infections and antimicrobial resistance in 2019

doi:10.21203/rs.3.rs-4057357/v1

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Global burden of Klebsiella pneumoniae infections and antimicrobial resistance in 2019

https://doi.org/10.21203/rs.3.rs-4057357/v1

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Purpose: To better target interventions against Klebsiella pneumoniae(KP) infections and antimicrobial resistance (AMR), we analyzed the global burden of KP using 2019 worldwide, regional and national data.

Methods: The methodology employed in this study involved collecting data on KP infections and AMR from two reputable sources: the Global Burden of Disease Study (GBD) 2019 and the Global Burden of Antimicrobial Resistance 2019 study. The analysis was based on a vast compilation of 471 million records, which informed eight distinct modeling components.

Results: KP infections have resulted in approximately 800,000 deaths worldwide, 80% of which were attributed to AMR. Notably, lower respiratory tract infections, bloodstream infections, and intra-abdominal infections were identified as the primary infectious syndromes caused by KP, accounting for nearly 90% of KP-related deaths and exhibiting the highest age-standardized mortality rates. South Asia and sub-Saharan Africa showed the greatest incidence of fatalities linked to KP infections, with the latter region additionally displaying the highest number and rate of deaths associated with KP-AMR. The mortality attributed to AMR in KP patients was predominantly caused by resistance to carbapenems and third-generation cephalosporins, accounting for more than fifty percent of the reported deaths.

Conclusions: KP has emerged as a significant concern within the realm of public health, particularly in areas characterized by limited financial resources. To adequately confront this escalating predicament, it is imperative to execute specific interventions.

Death

disability-adjusted life years

global burden of disease

Klebsiella pneumoniae

antimicrobial resistance

Infectious diseases have long been recognized as prominent contributors to mortality rates and have consequently garnered considerable attention as a global public health concern [1, 2]. ESKAPE organisms, the most prevalent pathogens responsible for healthcare-associated infections, include Enterococcus faecium, Staphylococcus aureus, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, and Enterobacter spp. The WHO has designated these pathogens priorities 1 and 2 due to their resistance to multiple drugs [3]. Consequently, the prevalence of these conditions has led to significant increases in morbidity and mortality rates, posing a formidable health challenge and imposing substantial financial burdens on numerous nations worldwide [4, 5].

As a member of the ESKAPE pathogens, KP can cause severe infections such as pneumonia, bloodstream infections, and neonatal and intensive care infections, thus posing a global threat to health and sustainable development [6]. Despite recent research publications addressing the consequences of bacterial infections and drug resistance on disease burden [7-10], studies concentrating on the culpability of individual bacteria in disease causation are rare. The WHO and the Maternal and Child Epidemiology Estimation have furnished worldwide estimations regarding the prevalence of Streptococcus pneumoniae and Haemophilus influenzae type b disease among children [11]. Additionally, in 2014, estimations were made regarding the global instances of antibiotic-resistant infections caused by Escherichia coli and KP[12]. However, insufficient evaluations of the global ramifications of KP infections and KP-AMR, along with the emergence of patterns in bacterial drug resistance, significantly hinder the prioritization of public health initiatives.

Our study aimed to conduct a comprehensive analysis of the global ramifications of KP infections and AMR in 2019. This analysis encompassed eight distinct infectious syndromes and six combinations of pathogens and drugs. To estimate the extent of infections and AMR caused by KP on a global, regional, and national scale, we gathered information from the GBD 2019.

Data sources

The data regarding the quantity and prevalence of fatalities related to KP infections and AMR were obtained from the GBD 2019 (http://ghdx.healthdata.org/gbd-2019) and the Antimicrobial Resistance 2019 studies (https://www.healthdata.org/research-analysis/health-risks-issues/antimicrobial-resistance-amr). The GBD study is an extensive collaborative research dataset encompassing all member countries of the WHO, offering epidemiological insights from 204 territories or countries. This comprehensive dataset includes information on 369 disorders and 87 associated risk factors [13]. To assess the magnitude of AMR, a total of 471 million separate records or samples were gathered, encompassing a range of factors, including multiple causes of mortality, hospital discharge, minimally invasive tissue sampling, comprehensive analysis of published studies, and microbiology laboratory findings obtained from both domestic and international surveillance systems [7]. These extensive datasets were utilized to identify eight modeling components, which were subsequently used to estimate the burden of KP infections and its association with AMR [8].

ICD codes for cancers

The appendix accompanying this study provides critical information on the corresponding ICD codes for each disease analyzed.

Related terms

GBD 2019 is defined by the following terms:

Years of life lost (YLLs): years lost resulting from premature mortality.

Years lived with disability (YLDs): the total number of years an individual lives with a condition that limits their ability to function at total capacity.

Disability-adjusted life years (DALYs): the summation of years of life lost because of YLLs and YLDs.

Statistical analysis

The study was conducted in two phases. The initial phase encompassed the acquisition of data about infectious syndromes caused by KP through three modeling steps, which have been documented in a previous publication [8]. In the first stage, fatalities were identified where the infections contributed to the death. Subsequently, the proportion of fatalities attributable to the illness and its specific contagious condition was computed. Ultimately, the proportion of fatalities resulting from a contagious condition that can be attributed to a particular microorganism was determined to be [8]. The estimation of the burden of KP-AMR in the latter part encompasses five primary elements: the quantification of fatalities impacted by the infections, the proportion of infectious deaths associated with a specific infectious syndrome, the allocation of infectious syndrome deaths attributed to a particular pathogen, the percentage of a specific pathogen exhibiting resistance to a targeted antibiotic, and the supplementary risk of mortality or duration of an infection associated with this resistance. By adhering to these procedures, the assessment of the impact of AMR can be ascertained by considering two hypothetical scenarios: deaths attributed to AMR and fatalities associated with AMR, as previously documented [7]. The final estimations of the ranked values were computed utilizing the 2.5th and 97.5th percentiles from 1000 posterior samples, accompanied by 95% uncertainty intervals (UIs). Subsequently, the data were analyzed and compared across regions, countries, infection types, and drug-pathogen pairs using GraphPad Prism 9, with statistical significance defined as P < 0.05 (two-tailed).

The GBD study identified eight distinct categories of infections globally associated with KP. These categories include lower respiratory tract infections (LRIs) and related thoracic infections, bloodstream infections (BSIs), peritoneal and intra-abdominal infections (IAIs), urinary tract infections (UTIs) and pyelonephritis, meningitis and other bacterial infections affecting the central nervous system (CNS), endocarditis and other infections impacting the heart, bacterial skin and subcutaneous inflammation, and infections of the bones, joints, and associated organs.

Based on the study, it was determined that the infections caused by KP gave rise to eight distinct infectious syndromes, resulting in an estimated 800,000 fatalities (95% UI: 571,000-1,062,000) across all age groups (Table 1). Additionally, the age-standardized mortality rate (ASMR) for KP infectious syndromes in that particular year was calculated to be 10.6 (with a range of 7.7 to 14.2) per 100,000 people (Supplementary Table 1). Among the infectious syndromes caused by KP, the most prevalent were LRIs, which resulted in 276,000 (220,000-343,000) deaths; BSIs, which accounted for 265,000 (157,000-416,000) deaths; and IAIs, which caused 158,000 (103,000-234,000) deaths (Table 1). These three syndromes collectively contributed to nearly 90% of KP infections-related fatalities, amounting to a total of 700,000 deaths. Notably, LRIs, BSIs, and IAIs also exhibited the highest ASMRs: LRIs 3.85 (3.07-4.77), BSIs 3.85 (3.07-4.77), and IAIs 1.99 (1.30-2.94) per 100,000 population (Supplementary Table 1).

The prevalence of the eight KP infectious syndromes varied across 21 GBD regions, with South Asia reporting the highest fatality count of 191,000 (135,000-260,000) deaths, followed by sub-Saharan Africa and East Asia (Table 1). However, the ranking of ASMRs experienced a shift, with four regions in sub-Saharan Africa occupying the top position, followed by Oceania and South Asia (Supplementary Table 1). On the contrary, Australasia, Oceania, and the Caribbean had the lowest number of deaths from KP syndrome, with fewer than 6,000 deaths (Table 1). Moreover, Australasia exhibited the lowest ASMR, at 3.48 (2.34-4.99) per 100,000 people (Supplementary Table 1).

Figure 1 illustrates that India recorded the highest number of deaths attributed to KP infections, with 134,000 (94,000-186,000) fatalities across all age groups, followed by China with 72,000 (45,000-111,000) and Nigeria with 46,000 (34,000-59,000) (Figure 1A). In terms of the ASMR, the Central African Republic demonstrated the highest rate at 41.01 [29.24-55.90] per 100,000 inhabitants, trailed by Lesotho (40.09 [28.56-55.26]) and Guinea-Bissau (36.35 [27.25-48.22]). In contrast, Iceland exhibited the lowest incidence of ASMR for KP infections, with a rate of 2.97 [2.04-4.15] per 100,000 people, followed by Bermuda (3.16 [2.04-4.68]) and Switzerland (3.34 [2.30-4.65]) (Figure 1B).

Antimicrobial resistance is a significant and concerning threat, resulting in an estimated 642,000 (465,000-863,000) deaths associated with KP-AMR. Notably, 193,000 deaths were attributed solely to KP-AMR in 2019. The impact of KP-AMR exhibited variability across the subregions of the GBD, with sub-Saharan Africa experiencing the highest level of impact, resulting in 186,000 deaths (144,000-240,000). South Asia closely followed with 175,000 deaths (124,000-241,000), while Southeast Asia, East Asia, and Oceania reported 104,000 deaths (69,000-151,000) (Table 2). However, there was a shift in the ranking order, with sub-Saharan Africa emerging as the region with the highest mortality rate associated with KP-AMR across all age groups, at 17.29 (13.33-22.17) per 100,000 individuals. Central Europe, Eastern Europe, and Central Asia were closely related at 9.8 (6.49-14.17), and South Asia was closely related at 9.71 (6.88-13.35) (Table 2). Table 2 also presents the corresponding estimates of YLLs, DALYs, and YLDs resulting from KP-AMR.

LRIs, BSIs, and IAIs accounted for the majority of the global burden associated with KP-AMR across GBD super regions (Figures 2, 3). LRIs were the leading cause of AMR-related deaths in KP patients, except in sub-Saharan Africa and South Asia, where BSIs were the primary cause in all the other five super regions (Figures 2, 3). Furthermore, among the 21 GBD regions, South Asia had the highest number of deaths attributed to KP-AMR, with 175,000 (124,000-241,000) fatalities, while sub-Saharan Africa had the highest mortality rate across all age groups (Figure 4). Moreover, South Asia has emerged as the predominant region in terms of fatalities associated with KP-AMR across all eight infectious syndromes (Supplementary Figure 1, Supplementary Figure 2).

According to the GBD 2019 study, carbapenem resistance resulted in more than 55,000 deaths, while third-generation cephalosporins (3GCs) caused 50,000 fatalities, and fluoroquinolones led to 29,000 deaths. The fatalities resulting from infectious syndromes induced by KP-AMR exhibited geographical variation based on the combination of pathogens and drugs (Supplementary Table 2). South Asia consistently maintained the highest ranking in terms of mortality resulting from KP-AMR, encompassing all six combinations of pathogens and drugs and accounting for more than 50% of the deaths associated with carbapenem resistance. This percentage was nearly seven times greater than that of Southeast Asia, which secured the second position (Supplementary Table 2). The corresponding mortality rates for all age groups are presented in Supplementary Table 3.

Our study aimed to examine the global implications of KP infections and AMR, with a focus on regional disparities and six specific pathogen-drug combinations in 2019. The outcomes of our investigation are as follows: (1) KP infections resulted in 800,000 fatalities globally, 80% of which were attributed to AMR. (2) LRIs, BSIs, and IAIs accounted for nearly 90% of the deaths associated with KP infections and were among the top three causes of KP-AMR-related mortality. (3) The prevalence of KP infections and AMR varied significantly across countries and regions globally. (4) The highest fatality rates attributed to KP infections were observed in South Asia and sub-Saharan Africa, with the latter region experiencing the greatest number of deaths associated with AMR. (5) In the case of all six pathogen‒drug combinations, resistance to carbapenems and 3GCs contributed to more than 50% of the deaths caused by KP-AMR.

In light of our present knowledge, our research provides an initial comprehensive analysis of the global and regional implications of KP infections and AMR. In 2019, the burden of eight infectious syndromes caused by AMR was significantly impacted by KP. These syndromes include LRIs, BSIs, IAIs, UTIs, CNS infections, endocarditis, and skin and bone infections. Among these, LRIs, BSIs, and IAIs were responsible for 90% of the fatalities. KP can colonize the gastrointestinal and respiratory tracts of humans, leading to infections when the bacteria enter the bloodstream or other tissues [14]. Furthermore, hypervirulent KP exhibits significantly greater virulence than traditional KP and can spread to distant sites, particularly the ocular region, respiratory system, and central nervous system [15]. As a member of the ESKAPE pathogens, KP is a significant public health challenge in numerous countries worldwide [16, 17]. In 2019, it was the third most common fatal drug-resistant pathogen, surpassed only by Escherichia coli and Staphylococcus aureus in terms of mortality [7].

The incidence of KP infections and KP-AMR varies considerably across different regions worldwide. Low- and middle-income areas, such as sub-Saharan Africa and South Asia, bear the brunt of KP infections and KP-AMR compared to high-income areas. In recent studies, it has been reported that in low- and middle-income countries (LMICs) where AMR is on the rise, KP has been identified as the primary contributing factor to neonatal sepsis and mortality in the intensive care unit [18, 19]. The disproportionate burden of AMR in LMICs can be attributed to various factors, including increased usage of antimicrobial agents, unnecessary self-medication [20, 21], inadequate public health systems, limited access to effective antimicrobial agents [22], poor hygiene practices [23], and limited healthcare-associated infection prevention programs. However, there is a lack of sufficient data on AMR in LMICs due to inadequate surveillance, absence of standardized laboratory facilities, shortage of skilled personnel, and inadequate data management [24].

The majority of deaths caused by KP-AMR can be attributed to resistance to carbapenems and 3GCs. Initially, carbapenemase was reported in a single country or region between 2006 and 2007 [25]. However, these cases are now documented in all 21 GBD regions, with the annual incidence of carbapenem-resistant Enterobacterales cases increasing from 0.6 to 1.1 per 100,000 population from 2015 to 2021 [26]. Carbapenem-resistant KP was found in varying proportions among patients in China from 2007 to 2020, ranging from 0.9% to nearly 20% [27, 28]. While the incidence of carbapenem-resistant KP cases declined from 2016 to 2020, there was a notable increase in the United States between 2021 and 2022 [29]. In LMICs, more than one-third of hospital-acquired KP infections exhibit resistance to carbapenems, and nearly 80% are resistant to 3GCs [16]. Resistance to 3GCs has been associated with elevated in-hospital mortality rates, increased hospital expenses, prolonged hospital stays, and reduced chances of being discharged alive [30, 31]. The global dissemination of AMR has been impacted by the inadequate utilization of antimicrobial agents, difficulties accessing dependable healthcare, increasing human mobility, and environmental factors such as animal husbandry, food provision, and sewage control.

This study is constrained by two significant limitations. Firstly, the deficient surveillance systems in LMICs have yielded insufficient data, which, in turn, has led to the emergence of imprecise information and selection bias. Secondly, the diverse criteria utilized by various nations to discern between drug resistance and susceptibility may give rise to discrepancies in classifications.

In 2019, KP posed a significant threat to the overall health of the general population, particularly in LMICs. To address this escalating challenge, it is imperative to devise focused interventions, encompassing vaccination [32], fortification of local surveillance and health systems, and the exploration of novel treatments beyond antibiotics, such as phages and fecal microbiota transplantation [33, 34].

Acknowledgments

The study was funded by the National Natural Science Foundation of China (No. 81871645 to JSP) and the Natural Science Foundation of Fujian Province of China (No. 2022J02030 to JSP; No. 2021J011384 to HWS). The funder had no role in the design or conduct of the study; collection, management, analysis, or interpretation of the data; preparation, review, or approval of the manuscript; or decision to submit the manuscript for publication.

Author contributions

JSP was responsible for the design of the study and had full access to all the data. HWS, TEW, and BHF conducted the methodology, while GHY and MTJ performed the statistical analysis. JSP and HWS were responsible for writing the article, and each author reviewed and approved the final report.

Availability of Data

All the data are available if needed.

Ethics approval

The study utilized data from publicly available databases, and ethical approval was not needed.

Conflicts of interest

None.

Funding

The National Natural Science Foundation of China (No. 81871645) and the Natural Science Fund of China's Fujian Province (No. 2021J011384; No. 2022J02030) were used.

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Tables are available in the Supplementary Files section.

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You are reading this latest preprint version

Global burden of Klebsiella pneumoniae infections and antimicrobial resistance in 2019

Status:

Version 1

Abstract

Figures

Introduction

Methods

Results

Discussion

Conclusion

Declarations

Author contributions

Availability of Data

Ethics approval

Conflicts of interest

Funding

References

Tables

Additional Declarations

Supplementary Files

Status:

Version 1