Season and Temperature Effects on Bloodstream Infection Incidence in a Korean Tertiary Referral Hospital

Young Suk Sohn; Jung-Hyun Byun; Young Ah Kim; Dong Chun Shin; Kyungwon Lee

doi:10.5145/ACM.2020.23.1.33

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Sohn, Byun, Kim, Shin, and Lee: Season and Temperature Effects on Bloodstream Infection Incidence in a Korean Tertiary Referral Hospital

Original Article

Ann Clin Microbiol 2020;23(1):33-43.

Published online: 12 March 2020

DOI: https://doi.org/10.5145/ACM.2020.23.1.33

Season and Temperature Effects on Bloodstream Infection Incidence in a Korean Tertiary Referral Hospital

Young Suk Sohn¹, Jung-Hyun Byun², Young Ah Kim³, Dong Chun Shin⁴, Kyungwon Lee¹

^¹Department of Laboratory Medicine, Research Institute of Bacterial Resistance, Yonsei University College of Medicine, Seoul

^²Department of Laboratory Medicine, Gyeongsang National University Hospital, Gyeongsang National University College of Medicine, Jinju

^³Department of Laboratory Medicine, National Health Insurance Service Ilsan Hospital, Goyang

^⁴Department of Environmental Health Graduate School of Public Health, Yonsei University, Seoul, Korea

Received 8 September 2019 Revised 23 August 2019 Accepted 23 August 2019

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Background

The weather has well-documented effects on infectious disease and reports suggest that summer peaks in the incidences of gram-negative bacterial infections among hospitalized patients. We evaluated how season and temperature changes affect bloodstream infection (BSI) incidences of major pathogens to understand BSI trends with an emphasis on

Methods

Incidence rates of BSIs by Staphylococcus aureus, Enterococcus spp., Escherichia coli, Klebsiella pneumoniae, Acinetobacter spp., and Pseudomonas aeruginosa were retrospectively analyzed from blood cultures during 2008–2016 at a university hospital in Seoul, Korea according to the acquisition sites. Warm months (June–September) had an average temperature of ≥20 °C and cold months (December–February) had an average temperature of ≤5 °C.

Results

We analyzed 18,047 cases, where 43% were with community-onset BSI. E. coli (N = 5,365) was the most common pathogen, followed byEnterococcus spp. (N = 3,980),S. aureus (N = 3,075), K. pneumoniae (N = 3,043),Acinetobacter spp. (N = 1,657), andP. aeruginosa (N = 927). The incidence of hospital-acquired BSI byEnterococcus spp. was weakly correlated with temperature, and the median incidence was higher during cold months. The incidence of community-onset BSI by E. coli was higher in warm months and was weakly correlated with temperature.

Conclusion

We found seasonal or temperature-associated variation in some species-associated BSIs. This could be a useful information for enhancing infection control and public health policies by taking season or climate into consideration.

Keywords: Bloodstream infection, Climate change, Incidence, Seasonality

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Fig. 1.

Correlation between bloodstream infection (BSI) by gram-positive cocci and average monthly temperature from 2008–2016 based on Pearson's correlation coefficient. (a) Temperature (°C) vs. incidence rate of community-onset BSI by S. aureus (cases per 10⁵ patient days), y = 0.00337x+1.774, r = 0.0565, P = 0.5612. (b) Temperature (°C) vs. incidence rate of hospital-acquired BSI by S. aureus (cases per 10⁶ patient days), y = 0.0588x+29.781, r = 0.0444, P = 0.6484. (c) Temperature (°C) vs. incidence rate of community-onset BSI by Enterococcus spp. (cases per 10⁵ patient days), y = 0.0488x+9.558, r = 0.0952, P = 0.3273. (d) Temperature (°C) vs. incidence rate of hospital-acquired BSI by Enterococcus spp. (cases per 10⁶ patient days), y = −0.495x+59.061, r = −0.3020, P = 0.0015. CA, community-onset; HA, hospital-acquired; Temp., temperature.

Fig. 2.

Correlation between bloodstream infection (BSI) by gram-negative bacilli and average monthly temperature from 2008–2016 based on Pearson's correlation coefficient. (a) Temperature (°C) vs. incidence rate of community-onset BSI by E. coli (cases per 10⁵ patient days), y = 0.540x+52.754, r = 0.3304, P = 0.0005. (b) Temperature (°C) vs. incidence rate of hospital-acquired BSI by E. coli (cases per 10⁶ patient days), y = 0.128x+23.142, r = 0.1443, P = 0.1363. (c) Temperature (°C) vs. incidence rate of community-onset BSI by K. pneumoniae (cases per 10⁵ patient days), y = 0.193x+22.874, r = 0.1986, P = 0.0394. (d) Temperature (°C) vs. incidence rate of hospital-acquired BSI by K. pneumoniae (cases per 10⁶ patient days), y = 0.124x+20.931, r = 0.1094, P = 0.2596. CO, community-onset; HA, hospital-acquired; Temp., temperature.

Fig. 3.

Correlation between bloodstream infection (BSI) by glucose non-fermenters and average monthly temperature from 2008–2016. (a) Temperature (°C) vs. incidence rate of community-onset BSI by Acinetobacter spp. (cases per 10⁵ patient days), y = 0.0500x+2.065, r = 0.2100, P = 0.0292. (b) Temperature (°C) vs. incidence rate of hospital-acquired BSI by Acinetobacter spp. (cases per 10⁶ patient days), y = −0.121x+25.202, r = −0.1148, P = 0.2368. (c) Temperature (°C) vs. incidence rate of community-onset BSI by P. aeruginosa (cases per 10⁵ patient days), y = 0.000520x+0.455, r = 0.0137, P = 0.8879. (d) Temperature (°C) vs. incidence rate of hospital-acquired BSI by P. aeruginosa (cases per 10⁶ patient days), y = 0.0565x+8.814, r = −0.0957, P = 0.3241. CO, community-onset; HA, hospital-acquired; Temp., temperature.

Table 1.

Etiologic agents of bloodstream infections according to acquisition site (2008–2016)

Year	S. aureus			Enterococcus spp.			E. coli			K. pneumoniae			Acinetobacter spp.			P. aeruginosa
	Total	CO	HA CO/ HA	Total	CO	HA CO/ HA	Total	CO	HA CO/ HA	Total	CO	HA CO/ HA	Total	CO	HA CO/ HA	Total	CO	HA CO/ HA
2008	256	93	163 0.6	368	54	314 0.2	443	313	130 2.4	191	106	85 1.2	160	15	145 0.1	113	44	69 0.6
2009	338	109	229 0.5	365	45	320 0.1	494	340	154 2.2	263	147	116 1.3	247	15	232 0.1	175	50	125 0.4
2010	272	120	152 0.8	395	62	333 0.2	453	328	125 2.6	223	116	107 1.1	144	15	129 0.1	85	32	53 0.6
2011	395	114	281 0.4	508	54	454 0.1	586	346	240 1.4	430	195	235 0.8	164	17	147 0.1	102	47	55 0.9
2012	319	139	180 0.8	347	55	292 0.2	490	358	132 2.7	292	167	125 1.3	202	20	182 0.1	80	22	58 0.4
2013	369	112	257 0.4	508	102	406 0.3	619	461	158 2.9	413	206	207 1.0	240	29	211 0.1	94	30	64 0.5
2014	312	139	173 0.8	476	93	383 0.2	678	497	181 2.7	351	204	147 1.4	167	21	146 0.1	84	23	61 0.4
2015	373	167	206 0.8	461	84	377 0.2	766	559	207 2.7	403	230	173 1.3	171	23	148 0.2	95	35	60 0.6
2016	441	160	281 0.6	552	98	454 0.2	836	596	240 2.5	477	242	235 1.0	162	15	147 0.1	99	44	55 0.8
9 years	3,075	1,153	1,922 0.6	3,980	647	3,333 0.2	5,365	3,798	1,567 2.4	3,043	1,613 1	1,430 1.1	1,657	170	1,487 0.1	927	327	600 0.5

Abbreviation: CO, community-onset; HA, hospital-acquired.

Table 2.

Incidence of community-onset bloodstream infections according to acquisition site and seasonal changes

^Etiologic agents	Community-onset (cases per 10⁵ patient days)
	Warm months			Cold months P
	M	95% CI	IQR	M	95% CI	IQR
S. aureus	17.88	16.16–20.01	13.96–20.92	16.80	15.63–19.17	15.25–20.37 0.6769
Enterococcus spp.	0.98	0.61–1.25	0.51–1.48	0.87	0.66–1.12	0.60–1.26 0.6871
E. coli	60.40	54.90–77.60	53.10–81.30	52.70	47.80–55.80	41.10–61.50 0.0044
K. pneumoniae	28.20	25.00–32.50	20.90–33.70	22.50	20.10–26.10	17.00–27.90 0.0518
Acinetobacter spp.	3.34	1.74–4.01	1.68–5.07	1.68	0.00–3.38	0.00–3.84 0.0672
P. aeruginosa	0.35	0.19–0.70	0.17–0.85	0.40	0.33–0.69	0.31–0.78 0.5976

Abbreviation: M, median; CI, confidence interval; IQR, interquartile range.

Table 3.

Incidence of hospital-acquired bloodstream infections according to acquisition site and seasonal changes

Etiologic agents	Hospital-acquired (cases per 10⁶ patient days)
Etiologic agents	Warm months		Cold month		s P
M	95% CI	IQR	M	95% CI	IQR
S. aureus 29.10	24.90–33.70	22.50–37.10	26.90	23.60–32.70	20.80–34.70 0.6467
Enterococcus spp. 45.20	39.60–47.30	37.90–51.50	57.20	49.80–63.90	48.90–65.60 0.0021
E. coli 25.40	22.50–30.70	20.60–31.50	24.20	17.10–28.20	16.90–31.20 0.3241
K. pneumoniae 23.50	18.40–28.40	16.90–30.50	19.80	13.90–25.30	13.70–27.10 0.1965
Acinetobacter spp. 20.90	17.22–25.69	13.80–27.70	26.60	21.59–28.60	19.70–31.40 0.0956
P. aeruginosa 8.87	6.74–11.52	5.57–12.70	7.97	5.69–11.55	5.13–12.31 0.3241

Abbreviation: M, median; CI, confidence interval; IQR, interquartile range.

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