Prospective Study Open Access
Copyright ©The Author(s) 2017. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Crit Care Med. Feb 4, 2017; 6(1): 79-84
Published online Feb 4, 2017. doi: 10.5492/wjccm.v6.i1.79
Attributable cost of a nosocomial infection in the intensive care unit: A prospective cohort study
Binila Chacko, John Victor Peter, Medical ICU, Division of Critical Care, Christian Medical College, Vellore 632004, Tamil Nadu, India
Kurien Thomas, Department of Medicine, Pondicherry Institute of Medical Sciences, Puducherry 605014, India
Thambu David, Department of Medicine II, Christian Medical College, Vellore 632004, Tamil Nadu, India
Hema Paul, Hospital Infection Control Committee, Christian Medical College, Vellore 632004, Tamil Nadu, India
Lakshmanan Jeyaseelan, Department of Biostatistics, Christian Medical College, Vellore 632004, Tamil Nadu, India
Author contributions: Chacko B, Thomas K, David T and Peter JV contributed to conception and design of the study; Chacko B and Paul H were involved with data acquisition; Peter JV and Jeyaseelan L analysed the data; Chacko B and Peter JV interpreted the data and drafted the article; all authors critical revision and final approval of the version of the article to be published.
Institutional review board statement: The study was reviewed and approved by the Institutional Review Board at Christian Medical College, Vellore, India. IRB Min No. 10011.
Informed consent statement: All study participants, or their legal guardian, provided informed written consent prior to study enrollment.
Conflict-of-interest statement: There are no financial implications or conflict of interest to declare for any of the authors.
Data sharing statement: No additional data is available.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Correspondence to: John Victor Peter, MD, DNB, MAMS, FRACP, FJFICM, FCICM, FICCM, Professor and Head, Medical ICU, Division of Critical Care, Christian Medical College, Ida Scudder Road, Vellore 632004, Tamil Nadu, India. peterjohnvictor@yahoo.com.au
Telephone: +91-416-2282693 Fax: +91-416-2282035
Received: August 19, 2016
Peer-review started: August 22, 2016
First decision: September 28, 2016
Revised: October 27, 2016
Accepted: November 21, 2016
Article in press: November 22, 2016
Published online: February 4, 2017

Abstract
AIM

To study the impact of hospital-acquired infections (HAIs) on cost and outcome from intensive care units (ICU) in India.

METHODS

Adult patients (> 18 years) admitted over 1-year, to a 24-bed medical critical care unit in India, were enrolled prospectively. Treatment cost and outcome data were collected. This cost data was merged with HAI data collected prospectively by the Hospital Infection Control Committee. Only infections occurring during ICU stay were included. The impact of HAI on treatment cost and mortality was assessed.

RESULTS

The mean (± SD) age of the cohort (n = 499) was 42.3 ± 16.5 years. Acute physiology and chronic health evaluation-II score was 13.9 (95%CI: 13.3-14.5); 86% were ventilated. ICU and hospital length of stay were 7.8 ± 5.5 and 13.9 ± 10 d respectively. Hospital mortality was 27.9%. During ICU stay, 76 (15.3%) patients developed an infection (ventilator-associated pneumonia 50; bloodstream infection 35; urinary tract infections 3), translating to 19.7 infections/1000 ICU days. When compared with those who did not develop an infection, an infection occurring during ICU stay was associated with significantly higher treatment cost [median (inter-quartile range, IQR) INR 92893 (USD 1523) (IQR 57168-140286) vs INR 180469 (USD 2958) (IQR 140030-237525); P < 0.001 and longer duration of ICU (6.7 ± 4.5 d vs 13.4 ± 7.0 d; P < 0.01) and hospital stay (12.4 ± 8.2 d vs 21.8 ± 13.9 d; P < 0.001)]. However ICU acquired infections did not impact hospital mortality (31.6% vs 27.2%; P = 0.49).

CONCLUSION

An infection acquired during ICU stay was associated with doubling of treatment cost and prolonged hospitalization but did not significantly increase mortality.

Key Words: Attributable cost, Nosocomial infection, Length of stay, Mortality, Intensive care

Core tip: There is paucity of data on the impact of hospital acquired infections (HAIs) on cost and outcome from intensive care units (ICU) in developing countries. In this prospective study of 499 patients admitted over 1-year to a medical ICU in India, there were 19.7 HAIs per 1000 ICU days. Occurrence of infection was associated with significantly higher treatment cost (P < 0.001); the median attributable cost of an infection was 87594 Rupees (USD 1436). Although ICU acquired infections increased ICU length of stay (6.7 ± 4.5 d vs 13.4 ± 7.0 d; P < 0.01), it did not impact mortality (31.6% vs 27.2%; P = 0.49).



INTRODUCTION

Health care associated infection (HAI) is a major preventable complication in critically ill patients across the world[1,2]. Whilst there is a significant body of information and evidence on the cost of these infections from developed countries, primary research from developing countries, in this area, is limited[3,4]. Translation of results of studies from developed countries on the impact and cost of infections to situations in developing countries may not be appropriate for several reasons: (1) different microbiological profile of HAIs[5,6]; (2) perceived reluctance among physicians regarding treatment of HAIs that is probably based on the impression that these infections are associated with poor survival[7,8]; and (3) limited resources and affordability which argues that resource allocation for the treatment of HAI would steal opportunities away from other potentially treatable patients, waiting for an intensive care unit (ICU) bed. The affordability issue is compounded by the fact that only about 10% of the estimated 70000 ICU beds in India are available in the public sector, where treatment is provided free of cost[9]. This poses a major problem of demand-supply mismatch, not only in the public sector, but also in the private sector since the population that needs to be covered in India is over 1 billion. Minimal subscription to private health insurance and resource pooling being in its infancy results in significant out-of-pocket expenses that push several families below the poverty line[10].

In the light of the above, a study was undertaken to evaluate the “cost” (in terms of money) and “impact” (in terms of clinical outcomes) of HAIs in developing countries. Such studies would facilitate investment on interventions that reduce infection as well as help plan appropriate allocation of the scarce resources of materials (ICU beds and equipment), manpower and money to address this problem in the ICU setting.

MATERIALS AND METHODS

In this study spanning 1-year, prospectively collected ICU cost data was merged with HAI data collected prospectively by the Hospital Infection Control Committee (HICC). ICU cost data was obtained from a study that looked at cost-utility as well as willingness-to-pay in patients admitted to the medical ICU[11].

Patients and setting

The study was undertaken in a 24-bed medical critical care unit in a 2500-bed, university-affiliated, private teaching hospital in semi-urban India. In this hospital, other than the very few covered by private health insurance, the entire treatment cost is expected to be paid for by the patient.

During a 1-year period (January-December 2011), adult patients (> 18 years) admitted to the 24-bed medical critical care unit were enrolled if they stayed beyond 24-h in the ICU. Patients not consenting to participate, patients not admitted under internal medicine (e.g., hematological malignancies, chronic liver disease), or patients with surgical problems were excluded. A diagnosis of HAI was made only when a new infection occurred 48-h after hospital admission. The study was approved by the Institutional Review Board and Ethics committee (IRB No. 10011) and consent was obtained from patient or next-of-kin.

Costs

“Treatment cost”, obtained from the hospital electronic system, was taken as the direct medical cost incurred from the time of admission to hospital until discharge from hospital (including ICU cost). This included bed and nursing charges, professional fees, equipment charges, investigations, oxygen charges, and medication costs[12].

Infections

Infection data was obtained from the HICC that does daily active surveillance. Only infections occurring during ICU stay were included. Ventilator associated pneumonia (VAP), blood stream infections (BSI) and urinary tract infections (UTI) developing 48-h after hospital admission were the infections that were analysed. VAP and UTI were defined as per the CDC guidelines[13]. BSI was defined as a positive blood culture with a recognized pathogen or the combination of clinical symptoms (fever > 38 °C, chills, hypotension) and two positive blood cultures for a common skin commensal from two separate blood samples drawn within 48 h[14].

Outcome data

The impact of infections on outcomes was explored. This included its effect on length of stay (ICU and hospital) and hospital mortality. We also assessed the impact of individual infections (VAP, UTI and BSI) on mortality.

Statistical analysis

Frequencies and percentages were used to describe baseline data, overall hospital and ICU mortality. Continuous variables [Acute physiology and chronic health evaluation (APACHE) II score, cost and ICU and hospital length of stay] were expressed as mean [standard deviation (SD)] if data was normally distributed. Where data was not normally distributed (e.g., treatment cost), it was expressed as median with interquartile range (IQR). Hospital mortality and length of stay (ICU and hospital) for the two groups, with HAI and without HAI, were calculated. χ2 tests were used to compare proportions. In order to study the impact of HAI on mortality, it was decided to adjust for disease severity and other potential confounders if mortality was significantly different between those who developed infection vs those who did not develop infection.

RESULTS
Baseline demographic data

During the study period, 1599 patients were admitted to medical critical care. A total of 499 patients were enrolled. Exclusion criteria were admission under other specialty units (n = 434), deaths or discharges within 24 h (n = 105), refusal of consent (n = 58) and those not recruited during public holidays or weekends (n = 503)[11].

Demographic data are summarized in Table 1. The diagnosis included 122 different International Classification of Diseases (ICD) code entities and comprised predominantly of acute febrile illness including scrub typhus (44.4%), deliberate self-harm (26%), neurological illnesses (9.8%) and cardiac problems (7.6%).

Table 1 Demographic data of the groups with and without hospital acquired infections.
FeaturesHAI (n = 76)No HAI (n = 420)P value
Age, mean (SD), (yr)39.4 (16.2)42.9 (16.5)0.04
Male:female46:30241:1790.70
APACHE II score, mean (SD)14.01 (4.7)13.9 (6.0)0.58
Diagnosis n (%)
Sepsis (including scrub typhus)27 (35.5)195 (46.4)
Deliberate self-harm30 (39.4)99 (23.6)
Cardiac4 (5.3)34 (8.1)0.11
Acute respiratory distress syndrome5 (6.6)28 (6.7)
Neurological6 (7.9)43 (10.2)
Others4 (5.3)21 (5.0)

The study cohort (n = 499) was relatively young with a mean (SD) age of 42.3 ± 16.5 years and mean APACHE-II of 13.9 (95%CI: 13.3-14.5); 86% of patients were invasively ventilated. The mean (SD) ICU length of stay was 7.8 ± 5.5 d.

Infection data

Infection data was available in 496 (99.4%) patients. During ICU stay, 76 patients (15.2%) developed an infection, translating to 19.7 infections/1000 ICU days. Patients who developed a HAI were significantly younger (P = 0.04) than those who did not develop a HAI (Table 1). However the gender distribution and APACHE-II score were not different between the groups. There were 50 episodes of VAP, 35 episodes of BSI and 3 episodes of UTI; 10 patients had more than one episode of infection. The median time to develop the infection followed an interesting pattern; VAP tended to occur in the first week of ICU stay (8 ± 5 d) while BSI occurred in the second week (11.4 ± 7 d) and UTI in the third week (18.7 ± 12.4 d).

Microbiological data

Overall, non-fermenting gram-negative carbapenem resistant organisms were isolated from 51 of the 88 episodes (36 VAP, 14 BSI and 1 UTI). There were 4 infections with colistin resistant organisms (3 VAP and 1 BSI). Twelve BSI isolates were susceptible gram-negative organisms. There was no Methicillin resistant staphylococcus aureus (MRSA) isolate in our cohort.

Outcome and cost data

Overall, infections were associated with doubling of length of stay (Table 2). However, mortality was similar in those who developed a HAI and those who did not develop it (Table 2). A logistic regression analysis was not performed in view of the lack of effect of infection on mortality. Additionally, when individual infections were considered separately, there was no mortality difference between those who developed a specific infection [i.e., VAP, BSI or catheter associated urinary tract infection (CAUTI)] vs those who did not develop any infection during ICU stay (Table 2).

Table 2 Impact of hospital-acquired infections on outcomes.
OutcomeHAI (n = 76)No HAI (n = 420)P value
ICU length of stay, mean (SD), (d)13.4 (7.0)6.7 (4.5)< 0.01
Hospital stay, mean (SD), (d)21.8 (13.9)12.4 (8.2)< 0.001
In-hospital mortality31.60%27.20%0.49
Mortality with VAP126%27.2%21.0
Mortality due to BSI137%27.2%20.24
CAUTI mortality133%27.2%21.0

An infection acquired in the ICU was associated with doubling of overall cost when compared with patients who did not develop an infection during hospitalization. When VAP, BSI and UTI were analysed independently, the overall cost (median IQR) of each infection was almost similar (Table 3). The median attributable cost of an infection worked out to INR 87594 (USD 1436).

Table 3 Comparison of overall cost between those with infection and those without infection.
TypeHAI (n = 76)No HAI1 (n = 420)Cost differenceP value
Mean (SD) cost (INR)
Any infection226398 (226268)115058 (93754)111340< 0.0001
VAP235350 (253421)115058 (93754)120292< 0.001
BSI283887 (341916)115058 (93754)168829< 0.001
CAUTI190059 (34096)115058 (93754)1559630.05
Median (IQR) cost (INR)
Any infection180469 (140030-237525)92875 (57243-139104)87594< 0.0001
VAP182991 (133038-238952)92875 (57243-139104)90116< 0.0001
BSI170753 (141788-238650)92875 (57243-139104)77878< 0.0001
CAUTI173085 (155818-190352)92875 (57243-139104)802100.06
DISCUSSION

This study provides insight and information on the burden (economic and otherwise) of common HAIs in the medical ICU of a developing country. While it could be argued that there is data from developed countries to this effect, our data with the different spectrum of infections (predominant VAP and few UTI) and microbiology (over 60% of the isolates carbapenem resistant) merit reporting and discussion.

Nosocomial infections, individually and overall in our study, were associated with doubling of cost without any impact on mortality. The acquisition of infection was also associated with the need for an additional 7-10 d in the ICU, resulting in further constraining the already limited ICU resources in our setting. Although the increased length of ICU stay is consistent with the limited evidence available for VAP in other countries[15], this has significant hospital infrastructure and public health implications in our setting.

These findings beg a response to the following questions. First, given the lack of impact of infections on mortality despite the antimicrobial resistance patterns, it is worth treating these infections. Second, should there be a focused approach to looking at measures to decrease infections and improving quality of patient care in ICU? On the face of it, the appropriate response to the above questions would be a resounding yes. However as alluded to, in view of the limited resources, treatment of patients with ICU acquired infections is likely to impact bed allocation to a patient with a more reversible problem. This, coupled with the inability to pay for the entire cost of treatment[11], places an additional economic burden on institutions that provide subsidy or charity. Denying on-going care for a potentially reversible problem (in this case a HAI) would violate ethical and moral principles of healthcare. Thus, the response to the second question assumes greater importance.

In India, ICU infrastructure and staffing are varied across hospitals[16]. It is also known that nosocomial infection rates in developing countries are far higher than that in developing countries. Focusing on reducing the incidence of nosocomial infections would translate to better utilization of ICU beds and economic resources. In addition to rigid enforcement of hand hygiene measures, micromanaging central line handling and optimizing pneumonia prevention strategies may help reduce infection rates. In addition, hospital administrators need to consider optimizing staff-patient ratio and spacing between ICU beds, a problem that probably potentiates infection risk[17,18]. The latter strategy would involve a cost shift from the patient (who bears the cost of an infection) to the hospital (in improving nursing ratio and bed spacing) that may be beyond the reach of many institutions.

This study, in the setting of a developing country, establishes the fact that an ICU acquired infection is associated with a significant increase in cost. The perception of poor survival is misplaced and patients who develop a HAI should be treated with cautious optimism. The utilitarian philosophy and steal phenomenon remains, since infections are associated with doubling of hospital stay and costs and are likely to prevent other patients from being treated in ICU. Efforts should be maximized on improving infection control practices since additional resource allocation in this setting may be challenging to the majority of health care settings.

COMMENTS
Background

Intensive care units (ICU) acquired infections are generally viewed with skepticism for several reasons. First, is a fact that treatment of ICU acquired infections would increase cost significantly and add pressure on the already stretched ICU resources second, is a perception that such infections would be associated with poor survival and third is an utilitarian philosophy that argues that such resource allocation would “steal” opportunities away from potentially treatable patients waiting for an ICU bed. This study aimed to explore the impact of ICU acquired infections on overall cost and mortality in a tertiary care hospital in a developing country. In this study spanning 1-year, prospectively collected ICU cost data incorporating direct and indirect cost was merged with nosocomial infection data collected by the hospital infection control committee.

Research frontiers

Health care associated infection (HAI) is a major preventable complication in critically ill patients across the world. Whilst there is a significant body of information and evidence on the cost of these infections from developed countries, primary research from developing countries, in this area, is limited. Additionally, translation of data from developed countries on the impact and cost of infections to situations in developing countries may not be appropriate given the different microbiological profile of HAIs.

Innovations and breakthroughs

This study has provided important information that suggests that paying attention to reducing nosocomial infections would not only translate to lower costs, but also make more intensive care beds available for other patients needing them.

Applications

This study provides insight and information on the burden (economic and otherwise) of common HAIs in the medical ICU of a developing country. While we were not surprised with the finding that HAIs were associated with doubling of cost as compared to those without HAIs, it was reassuring to know that there was no evidence of association of increased mortality despite the antimicrobial resistance patterns. It is thus worth treating this infections and there should be an aggressive focused approach to decrease infections and improve quality of patient care in ICU.

Terminology

HAIs are defined as new infections that develop in the hospital after 48 h of admission. In this study, cost and impact on outcomes (death and length of stay) of common ICU acquired infections, ventilator associated pneumonia, blood stream infections and urinary tract infections were analysed.

Peer-review

The work is novel and good.

Footnotes

Manuscript source: Invited manuscript

Specialty type: Critical care medicine

Country of origin: India

Peer-review report classification

Grade A (Excellent): A

Grade B (Very good): 0

Grade C (Good): C

Grade D (Fair): 0

Grade E (Poor): 0

P- Reviewer: Durandy YD, Mitra A S- Editor: Ji FF L- Editor: A E- Editor: Li D

References
1.  Dudeck MA, Weiner LM, Allen-Bridson K, Malpiedi PJ, Peterson KD, Pollock DA, Sievert DM, Edwards JR. National Healthcare Safety Network (NHSN) report, data summary for 2012, Device-associated module. Am J Infect Control. 2013;41:1148-1166.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 256]  [Cited by in F6Publishing: 233]  [Article Influence: 21.2]  [Reference Citation Analysis (0)]
2.  Rosenthal VD, Maki DG, Mehta Y, Leblebicioglu H, Memish ZA, Al-Mousa HH, Balkhy H, Hu B, Alvarez-Moreno C, Medeiros EA. International Nosocomial Infection Control Consortium (INICC) report, data summary of 43 countries for 2007-2012. Device-associated module. Am J Infect Control. 2014;42:942-956.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 157]  [Cited by in F6Publishing: 172]  [Article Influence: 17.2]  [Reference Citation Analysis (0)]
3.  Zimlichman E, Henderson D, Tamir O, Franz C, Song P, Yamin CK, Keohane C, Denham CR, Bates DW. Health care-associated infections: a meta-analysis of costs and financial impact on the US health care system. JAMA Intern Med. 2013;173:2039-2046.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1128]  [Cited by in F6Publishing: 1148]  [Article Influence: 104.4]  [Reference Citation Analysis (0)]
4.  Nangino Gde O, Oliveira CD, Correia PC, Machado Nde M, Dias AT. Financial impact of nosocomial infections in the intensive care units of a charitable hospital in Minas Gerais, Brazil. Rev Bras Ter Intensiva. 2012;24:357-361.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 9]  [Cited by in F6Publishing: 13]  [Article Influence: 1.2]  [Reference Citation Analysis (0)]
5.  Vincent JL, Rello J, Marshall J, Silva E, Anzueto A, Martin CD, Moreno R, Lipman J, Gomersall C, Sakr Y. International study of the prevalence and outcomes of infection in intensive care units. JAMA. 2009;302:2323-2329.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 2205]  [Cited by in F6Publishing: 2202]  [Article Influence: 146.8]  [Reference Citation Analysis (0)]
6.  Pradhan NP, Bhat SM, Ghadage DP. Nosocomial infections in the medical ICU: a retrospective study highlighting their prevalence, microbiological profile and impact on ICU stay and mortality. J Assoc Physicians India. 2014;62:18-21.  [PubMed]  [DOI]  [Cited in This Article: ]
7.  Pittet D, Tarara D, Wenzel RP. Nosocomial bloodstream infection in critically ill patients. Excess length of stay, extra costs, and attributable mortality. JAMA. 1994;271:1598-1601.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 225]  [Cited by in F6Publishing: 380]  [Article Influence: 12.7]  [Reference Citation Analysis (0)]
8.  Smith RL, Meixler SM, Simberkoff MS. Excess mortality in critically ill patients with nosocomial bloodstream infections. Chest. 1991;100:164-167.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 144]  [Cited by in F6Publishing: 154]  [Article Influence: 4.7]  [Reference Citation Analysis (0)]
9.  Divatia JV, Iyer S. Ten major priorities for intensive care in India. Intensive Care Med. 2015;41:1468-1471.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 5]  [Cited by in F6Publishing: 5]  [Article Influence: 0.6]  [Reference Citation Analysis (0)]
10.  Jayaram R, Ramakrishnan N. Cost of intensive care in India. Indian J Crit Care Med. 2008;12:55-61.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 37]  [Cited by in F6Publishing: 43]  [Article Influence: 3.1]  [Reference Citation Analysis (0)]
11.  Thomas K, Peter JV, Christina J, Jagadish AR, Rajan A, Lionel P, Jeyaseelan L, Yadav B, John G, Pichamuthu K. Cost-utility in medical intensive care patients. Rationalizing ongoing care and timing of discharge from intensive care. Ann Am Thorac Soc. 2015;12:1058-1065.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 6]  [Cited by in F6Publishing: 6]  [Article Influence: 0.8]  [Reference Citation Analysis (0)]
12.  Peter JV, Thomas K, Jeyaseelan L, Yadav B, Sudarsan TI, Christina J, Revathi A, John KR, Sudarsanam TD. COST OF INTENSIVE CARE IN INDIA. Int J Technol Assess Health Care. 2016;1-5.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 9]  [Cited by in F6Publishing: 9]  [Article Influence: 1.1]  [Reference Citation Analysis (0)]
13.  Horan TC, Andrus M, Dudeck MA. CDC/NHSN surveillance definition of health care-associated infection and criteria for specific types of infections in the acute care setting. Am J Infect Control. 2008;36:309-332.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 4031]  [Cited by in F6Publishing: 4399]  [Article Influence: 274.9]  [Reference Citation Analysis (0)]
14.  Suetens C, Morales I, Savey A, Palomar M, Hiesmayr M, Lepape A, Gastmeier P, Schmit JC, Valinteliene R, Fabry J. European surveillance of ICU-acquired infections (HELICS-ICU): methods and main results. J Hosp Infect. 2007;65 Suppl 2:171-173.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 81]  [Cited by in F6Publishing: 83]  [Article Influence: 4.9]  [Reference Citation Analysis (0)]
15.  Safdar N, Dezfulian C, Collard HR, Saint S. Clinical and economic consequences of ventilator-associated pneumonia: a systematic review. Crit Care Med. 2005;33:2184-2193.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 729]  [Cited by in F6Publishing: 707]  [Article Influence: 37.2]  [Reference Citation Analysis (0)]
16.  Yeolekar ME, Mehta S. ICU care in India--status and challenges. J Assoc Physicians India. 2008;56:221-222.  [PubMed]  [DOI]  [Cited in This Article: ]
17.  Schwab F, Meyer E, Geffers C, Gastmeier P. Understaffing, overcrowding, inappropriate nurse: ventilated patient ratio and nosocomial infections: which parameter is the best reflection of deficits? J Hosp Infect. 2012;80:133-139.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 60]  [Cited by in F6Publishing: 64]  [Article Influence: 4.9]  [Reference Citation Analysis (0)]
18.  Stone PW, Pogorzelska M, Kunches L, Hirschhorn LR. Hospital staffing and health care-associated infections: a systematic review of the literature. Clin Infect Dis. 2008;47:937-944.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 71]  [Cited by in F6Publishing: 66]  [Article Influence: 4.1]  [Reference Citation Analysis (0)]