<i>Clostridioides difficile</i> toxin positivity prolongs hospital stay and increases costs for critically ill patients in emergency patients

Abstract

Abstract:

ObjectiveTo explore the influence ofClostridioides difficile (C. difficile)positivity on clinical outcomes and identify associated risk factors in intensive care unit（ICU） patients.MethodsA retrospective analysis was conducted on 2 036 patients admitted to the emergency ICU of Ruijin Hospital from 2013 to 2022, comparing outcomes betweenC. difficile-positive (n=225) andC. difficilenegative (n=1 811) groups. Multivariate regression analysis was used to identify risk and protective factors.ResultsSignificantly prolonged hospital stays (B=18.734 d, 95% CI: 14.683-22.785) and higher treatment costs (B=68 854.912, 95% CI: 46 579.159-91 130.665) in theC. difficile-positive group, with no statistically significant difference in mortality between groups. Multivariate analysis identified carbapenem use (OR=1.58, 95% CI: 1.16-2.15), bloodstream infection (OR=1.77, 95% CI: 1.17-2.66), and biliary tract infection (OR=1.79, 95% CI: 1.03-3.10) as risk factors forC. difficilepositivity. Protective factors included metronidazole use (OR=0.58, 95% CI: 0.40-0.84), cephalosporin use (OR=0.54, 95% CI: 0.39-0.74), and female sex (OR=0.60, 95% CI： 0.44-0.83).ConclusionsC. difficilepositivity in critically ill patients did not affect mortality but prolonged hospitalization and increased costs. Both risk and protect factors forC. difficileare identified.

Key words:Clostridioides difficile,Intensive care unit,Antimicrobial stewardship,Infection prevention

CLC Number:

R515

YU Meiling, LI Jiaoyan, LI Jian, CHEN Ying, ZHAO Bing, MAO Enqiang, YANG Zhitao.Clostridioides difficiletoxin positivity prolongs hospital stay and increases costs for critically ill patients in emergency patients[J]. Journal of Internal Medicine Concepts & Practice, 2025, 20(03): 216-223.

Figures/Tables5

Figure 1

Table 1

Baseline characteristics of CDP and CDN patients [n(%)/M(P25,P75)]

项目	CDN组(n=1 811)	CDP组(n=225)	χ²/Z	P
年龄（岁）	55 (39, 69)	56 (39, 69)	-0.38	0.701
女性[n(%)]	664 (36.66)	58 (25.78)	10.36	0.001
APACHE Ⅱ	11.00 (7.00, 16.00)	11.00 (7.00, 17.00)	-1.24	0.217
既往病史[n(%)]
冠心病	126 (6.96)	19 (8.44)	0.67	0.415
脑卒中	118 (6.52)	18 (8.00)	0.70	0.402
急性胰腺炎	150 (8.29)	27 (12.00)	3.47	0.062
消化道溃疡	48 (2.65)	5 (2.22)	0.15	0.703
实验室指标
白细胞计数(×10⁹)	10.90 (7.67, 14.71)	11.23 (7.60, 15.93)	-1.26	0.207
C反应蛋白（mg/L）	106.00(23.00,201.70)	83.00 (16.00, 194.00)	-1.56	0.120
肌酐(μmol/L)	73.00 (54.00, 119.00)	77.00 (58.00, 132.00)	-1.28	0.201
白蛋白(g/L)	30.00 (26.00, 34.00)	30.00 (26.00, 34.00)	-1.20	0.229
血流感染[n(%)]	155 (8.56)	36 (16.00)	13.04	<0.001
中心静脉导管感染[n(%)]	140 (7.73)	25 (11.11)	3.07	0.080
胆道感染[n(%)]	84 (4.64)	19 (8.44)	6.04	0.014
住院治疗[n(%)]
禁食	1 389 (76.70)	168 (74.67)	0.46	0.498
肠内营养	1 291 (71.29)	163 (72.44)	0.13	0.717
生长抑素	534 (29.49)	63 (28.00)	0.21	0.644
质子泵抑制剂	1 445(79.79)	180(80.00)	0.05	0.941
免疫球蛋白	137 (7.56)	24 (10.67)	2.64	0.104
胸腺肽	97 (5.36)	10 (4.44)	0.33	0.563
SAID	751 (41.47)	102 (45.33)	1.23	0.268
NSAID	651 (35.95)	79 (35.11)	0.06	0.805
去甲肾上腺素	404 (22.31)	52 (23.11)	0.07	0.785
多巴胺	318 (17.56)	28 (12.44)	3.71	0.054
阿片类药物	425 (23.47)	57 (25.33)	0.39	0.535
CRRT	285 (15.74)	36 (16.00)	0.01	0.919
机械通气	537 (29.65)	76 (33.78)	1.62	0.203
抗菌药物
种类（种）	2 (2,3)	2 (1,4)	-1.41	0.160
青霉素[n(%)]	107 (5.91)	19 (8.44)	2.22	0.136
喹诺酮[n(%)]	493 (27.22)	48 (21.33)	3.56	0.059
碳青霉烯类[n(%)]	1 034 (57.10)	155 (68.89)	11.46	<0.001
万古霉素[n(%)]	516 (28.49)	86 (38.22)	9.10	0.003
利奈唑胺[n(%)]	304 (16.79)	31 (13.78)	1.32	0.251
阿米卡星[n(%)]	91 (5.02)	12 (5.33)	0.04	0.842
甲硝唑[n(%)]	692 (38.21)	50 (22.22)	22.09	<.001
磺胺甲唑[n(%)]	92 (5.08)	13 (5.78)	0.20	0.655
第1代头孢菌素[n(%)]	6(0.33)	0(0)	0.748	0.387
第2代头孢菌素[n(%)]	195 (10.77)	20(8.89)	0.748	0.387
第3代头孢菌素[n(%)]	1 150(63.50)	106(47.11)	22.75	<0.001
第4代头孢菌素[n(%)]	40(2.21)	14(6.22)	12.49	<0.001
替加环素[n(%)]	135 (7.45)	15 (6.67)	0.18	0.670
预后
住院时长 (d)	23.00 (15.00, 37.00)	39.00 (23.00, 66.00)	-8.88	<0.001
住院费用（元）	73 009.11 (41 605.92, 147 581.23)	127 163.58 (74 607.01, 262 362.70)	-8.24	<0.001
死亡[n(%)]	265 (14.63)	41 (18.22)	2.02	0.155

Table 1

Table 2

Multiple linear regression analysis of the impact of CDP on length of hospital stay

变量	未标准化系数		标准化系数	t	P	B的95%CI		共线性统计
变量	B	SE	β	t	P	下限	上限	容差	VIF
回归方程截距	26.570	2.639		10.069	0.000	21.395	31.745
年龄	-0.051	0.037	-0.032	-1.396	0.163	-0.123	0.021	0.896	1.116
CDP	18.734	2.066	0.196	9.069	0.000	14.683	22.785	0.998	1.003
冠心病	6.396	2.603	0.055	2.457	0.014	1.290	11.501	0.933	1.072
白细胞计数	0.305	0.108	0.062	2.822	0.005	0.093	0.517	0.973	1.027
C反应蛋白	0.028	0.006	0.101	4.525	0.000	0.016	0.040	0.931	1.075
R²	0.058
调整后R²	0.056
F	F(5，2 030)=25.115,P<0.001

Table 2

Table 3

Multiple linear regression analysis of the impact of CDP in hospitalization costs

变量	未标准化系数		标准化系数	t	P	B的95%CI		共线性统计
变量	B	SE	β	t	P	下限	上限	容差	VIF
回归方程截距	59 006.872	22 748.351		2.594	0.010	14 394.192	103 619.552
APACHE Ⅱ	3 994.021	577.936	0.164	6.911	0.000	2 860.608	5 127.434	0.807	1.239
CDP	68 854.912	11 358.579	0.130	6.062	0.000	46 579.159	91 130.665	0.994	1.006
急性胰腺炎	-26 425.580	13 032.176	-0.045	-2.028	0.043	-51 983.489	-867.671	0.935	1.069
白细胞计数	722.038	601.734	0.026	1.200	0.230	-458.047	1 902.123	0.948	1.055
C反应蛋白	157.321	33.133	0.103	4.748	0.000	92.342	222.299	0.968	1.033
肌酐	78.469	21.622	0.082	3.629	0.000	36.066	120.872	0.883	1.133
白蛋白	-497.693	625.675	-0.018	-0.795	0.426	-1 724.728	729.343	0.900	1.111
R²	0.080
调整后R²	0.077
F	F(7，2 028)=25.211,P<0.001

Table 3

Table 4

Multivariate regression analysis of risk factors for CDP

变量	变量水平	β	多因素回归分析OR(95% CI)	P
性别	女性	-0.500	0.60 (0.44 ~ 0.83)	0.002
	男性	对照
血流感染	阳性	0.570	1.77 (1.17 ~ 2.66)	0.007
	阴性	对照
胆道感染	阳性	0.580	1.79 (1.03 ~ 3.10)	0.039
	阴性	对照
碳青霉烯	使用	0.460	1.58 (1.16 ~ 2.15)	0.003
	未使用	对照
甲硝唑静脉注射	使用	-0.540	0.58 (0.40 ~ 0.84)	0.004
	未使用	对照
头孢菌素	使用	-0.620	0.54 (0.39 ~ 0.74)	<.001
	未使用	对照

Table 4

References33

[7]	Karanika S, Paudel S, Zervou FN, et al. Prevalence and clinical outcomes ofClostridium difficileinfection in the intensive care unit[J].Open Forum Infect Dis,2015,3(1):ofv186.
[8]	Loo VG, Poirier L, Miller MA, et al. A predominantly clonal multi-institutional outbreak ofClostridium difficile-associated diarrhea with high morbidity and mortality[J].N Engl J Med,2005,353(23):2442-2449.
[9]	Zahar JR, Schwebel C, Adrie C, et al. Outcome of ICU patients withClostridium difficileinfection[J].Crit Care,2012,16(6):R215.
[10]	Worley J, Delaney ML, Cummins CK, et al. Genomic determination of relative risks forClostridioides difficileinfection from asymptomatic carriage in Intensive Care Unit patients[J].Clin Infect Dis,2021,73(7):e1727-e1736. doi:10.1093/cid/ciaa894pmid:32676661
[11]	Longtin Y, Paquet-Bolduc B, Gilca R, et al. Effect of detecting and isolatingClostridium difficilecarriers at hospital admission on the incidence of C difficile infections[J].JAMA Intern Med,2016,176(6):796-804. doi:10.1001/jamainternmed.2016.0177pmid:27111806
[12]	Peterson LR, O’Grady S, Keegan M, et al. ReducedClostridioides difficileinfection in a pragmatic stepped-wedge initiative using admission surveillance to detect colonization[J].PLoS One,2020,15(3):e0230475.
[13]	Rao K, Malani PN. Diagnosis and treatment ofClostridioides(Clostridium)difficileinfection in adults in 2020[J].JAMA,2020,323(14):1403-1404.
[14]	Ang CW, Heyes G, Morrison P, et al. The acquisition and outcome of ICU-acquiredClostridium difficileinfection in a single centre in the UK[J].J Infect,2008,57(6):435-440.
[15]	Wang P, Zhou Y, Wang Z, et al. Identification ofClostridium difficileribotype 027 for the first time in Mainland China[J].Infect Control Hosp Epidemiol,2014,35(1):95-98.
[16]	Zhou Y, Mao L, Yu J, et al. Epidemiology ofClostridium difficileinfection in hospitalized adults and the first isolation ofC. difficilePCR ribotype 027 in central China[J].BMC Infect Dis,2019,19(1):232. doi:10.1186/s12879-019-3841-6pmid:30845918
[17]	Trubiano JA, Cheng AC, Korman TM, et al. Australasian Society Of Infectious Diseases updated guidelines for the management ofClostridium difficileinfection in adults and children in Australia and New Zealand[J].Intern Med J,2016,46(4):479-493. doi:10.1111/imj.13027pmid:27062204
[18]	中华医学会外科学分会, 中国研究型医院学会感染性疾病循证与转化专业委员会. 中国艰难梭菌感染诊治及预防指南(2024)[J].中华外科杂志,202,62(10):893-908.
[19]	Lawrence SJ, Puzniak LA, Shadel BN, et al.Clostridium difficilein the intensive care unit: epidemiology, costs, and colonization pressure[J].Infect Control Hosp Epidemiol,2007,28(2):123-130.
[20]	Martin SS, Aday AW, Almarzooq ZI, et al.2024heart disease and stroke statistics: a report of US and global data from the American Heart Association[J].Circulation,2024,149(8):e347-e913. doi:10.1161/CIR.0000000000001209pmid:38264914
[21]	Le Monnier A, Duburcq A, Zahar JR, et al. Hospital cost ofClostridium difficileinfection including the contribution of recurrences in French acute-care hospitals[J].J Hosp Infect,2015,91(2):117-122. doi:10.1016/j.jhin.2015.06.017pmid:26253518
[22]	Zhang S, Palazuelos-Munoz S, Balsells EM, et al. Cost of hospital management ofClostridium difficileinfection in United States-a meta-analysis and modelling study[J].BMC Infect Dis,2016,16(1):447.
[23]	Jones AM, Kuijper EJ, Wilcox MH.Clostridium difficile: a European perspective[J].J Infect,2013,66(2):115-128. doi:10.1016/j.jinf.2012.10.019pmid:23103666
[24]	Kahraman F, Yılmaz AS, Demir M, et al. APACHE Ⅱ score predicts in-hospital mortality more accurately than inflammatory indices in patients with acute coronary syndrome[J].Kardiologiia,2022,62(9):54-59. doi:10.18087/cardio.2022.9.n1979pmid:36206138
[25]	Mouliou DS. C-reactive protein: pathophysiology, diagnosis, false test results and a novel diagnostic algorithm for clinicians[J].Diseases,2023,11(4):132.
[26]	Morrison DJ, Preston T. Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism[J].Gut Microbes,2016,7(3):189-200. doi:10.1080/19490976.2015.1134082pmid:26963409
[27]	Buffie CG, Bucci V, Stein RR, et al. Precision microbiome reconstitution restores bile acid mediated resistance toClostridium difficile[J].Nature,2015,517(7533):205-208.
[28]	Maffei S, Forini F, Canale P, et al. Gut microbiota and sex hormones: crosstalking players in cardiometabolic and cardiovascular disease[J].Int J Mol Sci,2022,23(13):7154.
[1]	Quan M, Zhang X, Fang Q, et al. Fighting againstClostridioides difficileinfection: current medications[J].Int J Antimicrob Agents,2024,64(1):107198.
[2]	Salvati F, Catania F, Murri R, et al.Clostridioides difficileinfection: an update[J].Infez Med,2024,32(3):280-291.
[3]	Prechter F, Katzer K, Bauer M, et al. Sleeping with the enemy:Clostridium difficileinfection in the intensive care unit[J].Crit Care,2017,21(1):260.
[4]	Lee CC, Chiu CW, Lee JC, et al. Risk factors and clinical impact of carbapenem-resistant enterobacterales coinfections among hospitalized patients withClostridioides difficileinfection[J].Infect Drug Resist,2022,15:6287-6295.
[5]	Dubberke ER, Olsen MA. Burden ofClostridium difficileon the healthcare system[J].Clin Infect Dis,2012,55 Suppl2:S88-S92.
[6]	Lessa FC, Winston LG, McDonald LC, et al. Burden ofClostridium difficileinfection in the United States[J].N Engl J Med,2015,372(24):2369-2370.
[29]	Miller MA, Louie T, Mullane K, et al. Derivation and validation of a simple clinical bedside score (ATLAS) forClostridium difficileinfection which predicts response to therapy[J].BMC Infect Dis,2013,13:148.
[30]	Brown KA, Khanafer N, Daneman N, et al. Meta-analysis of antibiotics and the risk of community-associatedClostridium difficileinfection[J].Antimicrob Agents Chemother,2013,57(5):2326-2332.
[31]	McDonald LC, Gerding DN, Johnson S, et al. Clinical practice guidelines forClostridium difficileinfection in adults and children: 2017 update by the Infectious Diseases Society of America (IDSA) and Society for Healthcare Epidemiology of America (SHEA)[J].Clin Infect Dis,2018,66(7):e1-e48.
[32]	Slimings C, Riley TV. Antibiotics and hospital-acquiredClostridium difficileinfection: update of systematic review and meta-analysis[J].J Antimicrob Chemother,2014,69(4):881-891. doi:10.1093/jac/dkt477pmid:24324224
[33]	Wren CM, Cowper J, Greer N, et al. Effect of reduced fluoroquinolone use on cephalosporin use, susceptibilities andClostridioides difficileinfections[J].Antibiotics (Basel),2022,11(10):1312.

Clostridioides difficiletoxin positivity prolongs hospital stay and increases costs for critically ill patients in emergency patients

RichHTML

PDF (PC)

Knowledge

Abstract

Cite this article

share this article

Figures/Tables5

References33

Related Articles15

Recommended Articles

Metrics

Comments

[1]	TAN Ruoming, QU Hongping.Prevention and control of multidrug-resistant bacteria infection in surgical patients[J]. Journal of Surgery Concepts & Practice, 2023, 28(05): 420-424.
[2]	CUI Jiasong, ZHANG Enming, WANG Suxing, GAN Lu, DAI Zhengyue, FANG Qiong.The current status of intensive care unit competency and infectious disease emergency response capability of nurses involved in the critical care of COVID-19 in Shanghai[J]. Journal of Internal Medicine Concepts & Practice, 2023, 18(01): 43-47.
[3]	SHI Yingying, ZHONG Xu, LIU Jialin, HE Le, XIONG Shaoji, WENG Y, DING Chengwei, YANG Y, CHEN Weihon, QIU Liping, XIN Haiguang.Hospital infection prevention and control practices in anti-epidemic medical staff and workers during COVID-19 epidemic: investigation and countermeasures[J]. Journal of Diagnostics Concepts & Practice, 2022, 21(02): 178-183.
[4]	ZHANG Yibo, WU Wenjuan, BI Yufang, JING Feng, GU Zhidong, YANG Zhitao, SHANG Hanbing, LIN Jingsheng, CHEN Erzhen.Construction and practice of infection prevention and control system in large Fangcang shelter hospitals[J]. Journal of Diagnostics Concepts & Practice, 2022, 21(02): 165-168.
[5]	LI Li, ZHU Yongzhen, ZHOU Min, QIAN Jia, FANG Lili.Clinical isolates of multi drug resistant bacteria in a hospital from 2017 to 2021 in Jiading District of Shanghai[J]. Journal of Diagnostics Concepts & Practice, 2022, 21(01): 62-67.
[6]	WU Hao, FANG Hua, WANG Ruizhong, QU Jinghua, SHEN Xiaofeng, CHEN Huaping, GU Wenchao.Antimicrobial stewardship enhancing the submission rate of microbiological specimens before therapeutic use of antimicrobial agents[J]. Journal of Diagnostics Concepts & Practice, 2019, 18(1): 93-97.
[7]	.[J]. Journal of Internal Medicine Concepts & Practice, 2019, 14(02): 99-104.
[8]	LI Meiling, LI Lei, ZHANG ruyuan, LIU Jialin, QU Hongping.Impact of trace element supplementation on inflammatory response in postoperative patients with sepsis[J]. Journal of Surgery Concepts & Practice, 2018, 23(06): 533-538.
[9]	.[J]. Journal of Diagnostics Concepts & Practice, 2013, 12(04): 457-461.
[10]	.[J]. Journal of Internal Medicine Concepts & Practice, 2013, 8(03): 204-208.
[11]	.[J]. Journal of Internal Medicine Concepts & Practice, 2010, 5(02): 170-172.
[12]	.[J]. Journal of Diagnostics Concepts & Practice, 2009, 8(05): 487-491.
[13]	.[J]. Journal of Internal Medicine Concepts & Practice, 2008, 3(05): 347-350.
[14]	.[J]. Journal of Surgery Concepts & Practice, 2002, 7(02): 128-130.
[15]	.[J]. Journal of Surgery Concepts & Practice, 2000, 5(04): 257-259.