Case Study Scenario

ARTICLE

Nurse Staffing and NICU Infection Rates Jeannette A. Rogowski, PhD; Douglas Staiger, PhD; Thelma Patrick, PhD, RN; Jeffrey Horbar, MD; Michael Kenny, MS; Eileen T. Lake, PhD, RN

Importance: There are substantial shortfalls in nurse staffing in US neonatal intensive care units (NICUs) rela- tive to national guidelines. These are associated with higher rates of nosocomial infections among infants with very low birth weights.

Objective: To study the adequacy of NICU nurse staff- ing in the United States using national guidelines and ana- lyze its association with infant outcomes.

Design: Retrospective cohort study. Data for 2008 were collected by web survey of staff nurses. Data for 2009 were collected for 4 shifts in 4 calendar quarters (3 in 2009 and 1 in 2010).

Setting: Sixty-seven US NICUs from the Vermont Ox- ford Network, a national voluntary network of hospital NICUs.

Participants: All inborn very low-birth-weight (VLBW) infants, with a NICU stay of at least 3 days, discharged from the NICUs in 2008 (n=5771) and 2009 (n=5630). All staff-registered nurses with infant assignments.

Exposures: We measured nurse understaffing relative to acuity-based guidelines using 2008 survey data (4046 nurses and 10 394 infant assignments) and data for 4 com- plete shifts (3645 nurses and 8804 infant assignments) in 2009-2010.

Main Outcomes and Measures: An infection in blood or cerebrospinal fluid culture occurring more than 3 days after birth among VLBW inborn infants. The hypothesis was formulated prior to data collection.

Results: Hospitals understaffed 31% of their NICU in- fants and 68% of high-acuity infants relative to guide- lines. To meet minimum staffing guidelines on average would require an additional 0.11 of a nurse per infant overall and 0.34 of a nurse per high-acuity infant. Very low-birth-weight infant infection rates were 16.4% in 2008 and 13.9% in 2009. A 1 standard deviation–higher un- derstaffing level (SD, 0.11 in 2008 and 0.08 in 2009) was associated with adjusted odds ratios of 1.39 (95% CI, 1.19- 1.62; P� .001) in 2008 and 1.40 (95% CI, 1.19-1.65; P� .001) in 2009.

Conclusions and Relevance: Substantial NICU nurse understaffing relative to national guidelines is wide- spread. Understaffing is associated with an increased risk for VLBW nosocomial infection. Hospital administra- tors and NICU managers should assess their staffing decisions to devote needed nursing care to critically ill infants.

JAMA Pediatr. 2013;167(5):444-450. Published online March 18, 2013. doi:10.1001/jamapediatrics.2013.18

N EONATAL INTENSIVE CARE

units (NICUs) care for the most critically ill infants. Neonatal intensive care unit stays are among the

most expensive hospitalizations1 and re- quire high levels of nursing resources. Very little is known about the adequacy of staff- ing in US NICUs. Acuity-based staffing

guidelines for neonatal nursing2 were re- cently reaffirmed by national medical and nursing bodies,3,4 although definitions of infant acuity levels do not exist. It is not

known how well the guidelines are fol- lowed or how guideline adherence relates to infant outcomes.

The guidelines specify ranges of nurse to patient ratios across infant acuity levels, as well as requisite nurse training and ex- perience.For instance, infantswiththe low- estacuity levelshavearecommendednurse to patient ratio of 1 to 3 or 4. In contrast, the highest acuity infants have recom- mended ratios of 1 or more nurses per pa- tient. Furthermore, the guidelines also ad- dress the level of education and experience of thenurses,noting that“registerednurses in the NICU should have specialty certifi- cation or advanced training. They also shouldbeexperiencedincaringforunstable

For editorial comment see page 485

Author Aff Departmen and Policy, Health, Uni and Dentist Piscataway, Rogowski); Economics Hanover, N National Bu Research, C Massachuse College of N University, Patrick); D Pediatrics, Vermont (M Oxford Net Burlington, Center for H and Policy Nursing, D Sociology, L Institute of University Philadelphi

Author Affiliations are listed at the end of this article.

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neonates with multi-organ system problems and in spe- cialized care technology.”3(p32)

One patient outcome that has been directly linked to nurse staffing in critical care is infection.5,6 Most NICU infants have central venous lines. Nurse understaffing could result in lapses in aseptic technique that increase infants’ risk for infection.7,8 A study of 2 New York NICUs found that higher nurse staffing was associated with sig- nificantly lower infection risk in one NICU but not the other.9 Several other single-site NICU studies have shown that infection spread is associated with nurse staff- ing.10-13 A large British study found no association be- tween nurse staffing and infection among all NICU in- fants.14 However, another British study in 6 NICUs showed that more than half of shifts fell short of British guide- lines and that understaffing led to delays in essential treat- ment and reduced clinical care.15

The Affordable Care Act established the Center for Medicare and Medicaid Innovation to improve quality and reduce costs in health care through improvements in health system delivery and payment innovation. The Centers for Medicare and Medicaid Services has already reformed payments for hospital-associated infections under Medicaid. For hospitals to respond effectively to these incentives, they must have access to evidence about the health systems factors, such as nurse staffing, that contribute to adverse patient outcomes such as in- fection.

We developed definitions for the national NICU staff- ing guidelines and studied guideline adherence and its association with hospital-associated infection in very low- birth-weight (VLBW) infants. We hypothesized that nurse understaffing would be positively associated with noso- comial infection. Very low-birth-weight infants are the highest-risk pediatric population, accounting for half of infant deaths in the United States each year.16 They are highly susceptible to infection due to an underdevel- oped immune system, more transparent and penetrable skin barrier, and high prevalence of central lines.17-19 Hos- pital-associated infections in this population have been associated with poor neurodevelopmental and growth out- comes in early childhood, increased mortality, and lon-

ger hospital stay.20-22 Medicaid is the largest payer for the care of these infants.23

METHODS

STUDY DESIGN AND DATA

This retrospective cohort study was conducted in the Ver- mont Oxford Network (VON), a national voluntary hospital network dedicated to improving the quality and safety of NICU care. The VON database contains detailed uniform clinical and treatment information on all VLBW infants. By 2008, the US network comprised 578 hospitals, which included approximately 65% of NICUs and 80% of all VLBW infants. This study included 67 VON hospitals with inborn infants in 2008 and 2009, with nurse staffing data from 2 data collections.

The 2008 data were collected by web survey of staff nurses and included 4046 nurses assigned to 10 394 infants (response rate, 77%). Nurses reported on their last shift the infant assignment including infants’ acuity levels and whether infants were coassigned. The 2009 data were col- lected on 4 complete shifts. Data were collected for 4 shifts in 4 calendar quarters (3 in 2009 and 1 in 2010): 1 day shift and 3 shifts that were randomized to day, night, and week- end shifts (3645 nurses assigned to 8804 infants). For sim- plicity, these data are referred to as the 2009 data. Interrater reliability of the acuity levels was measured for 258 infants in 9 hospitals in 2009.

This project was approved by the institutional review boards of the University of Medicine and Dentistry of New Jersey, the University of Pennsylvania, the University of Vermont, Ohio State University, Dartmouth College, and the study hospitals.

VARIABLES

Definition of Infant Acuity Levels

The national guidelines that have existed since 1992 comprise 5 categories of infants. Infant acuity definitions were devel- oped to represent mutually exclusive categories of infant need for nursing resources (Table 1). An expert panel that in- cluded a neonatologist, a perinatal nurse specialist, and a rep- resentative from the National Association of Neonatal Nurses

Table 1. Definitions for Infant Acuity Levels

Level Care Provided per Newborn

Requirement According to Guideline3,4 Definition

1 Continuing care Infant only requiring PO or NG feedings, occasional enteral medications, basic monitoring (may or may not have a hep lock for medications)

2 Intermediate care Stable infant with established management plan, not requiring significant support Eg, room air, supplemental oxygen or low-flow nasal cannula, several medications

3 Intensive care Infant is stabilized, although requires frequent treatment and monitoring to assure maintenance of stability

Eg, ventilator, CPAP, high-flow nasal cannula, multiple intravenous needs via central or peripheral line

4 Multisystem support Infant requires continuous monitoring and interventions Eg, conventional ventilation, stable on HFV, continuous drug infusions, several intravenous fluid changes via central line

5 Unstable, requiring complex critical care Infant is medically unstable and vulnerable, requiring many simultaneous interventions Eg, ECMO, HFV, nitric oxide, frequent administration of fluids, medication

Abbreviations: CPAP, continuous positive airway pressure; ECMO, extracorporeal circulation membrane oxygenation; HFV, high-frequency ventilation; NG, nasogastric; PO, by mouth.

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developed the definitions. These were refined through focus groups and feedback from a broad range of neonatal nurses.

Nurse Staffing Measures

Guidelines for the nurse to patient ratio by acuity level were available from medical and nursing specialty societies.3(p29)4(p

33) Nurse to patient ratios by acuity were calculated for all in- fants in each NICU (adjusted for coassignments). Compliance was defined as meeting the minimum threshold. For 3 acuity levels (1, 2, and 3), the guideline specifies a range, and the maximum number of infants per nurse was used as the threshold. For acuity level 5, where the guideline indicates 1 or more nurses per infant, the threshold was set to 1 nurse per infant. When another nurse was coassigned, we assumed that the additional nurse was entirely available to care for the in- fant. This approach created a conservative estimate of under- staffing. There were few coassignments (3.3% in 2008 and 1.5% in 2009). Two measures of understaffing were created: the percentage of infants staffed below guidelines and the mean fraction of a nurse per infant needed to meet guidelines. Because the 2009 data were based on a census of all infants and nurses on a shift and the 2008 data were based on a nurse survey, the latter data were subject to measurement error. In the survey, nurses reported caring for 6% more infants and a slightly higher average infant acuity level, and there was more variation across nurses in patient load. Thus, survey-based measures are expected to be biased toward larger understaff- ing compared with complete shift data. The results based on the 2009 data were emphasized.

Infant characteristics, infection rates, and NICU-level mea- sures were obtained from the VON database using standard- ized definitions. The VON risk-adjustment model24 included gestational age in weeks (and its square); small for gestational age; 1-minute Apgar score; race and ethnicity (non-Hispanic

black, non-Hispanic white, or other [including Hispanic]); sex; multiple birth; presence of a major birth defect; vaginal deliv- ery; and whether the mother received prenatal care. This model had an area under the receiver operating characteristic curve of 0.76.

Risk-adjusted infection rates for all sites were computed for both years. Nosocomial infection was defined as an infec- tion in blood or cerebrospinal fluid culture occurring more than 3 days after birth for 3 culture-proven infections: coagu- lase-negative staphylococcus, the most common bacterial in- fection in the NICU; other bacterial infections; and fungal in- fections. In 2009, very few infants (0.12%) were transferred, contracted an infection, and were readmitted to the birth hos- pital where the infection was attributed.

Two NICU-level variables were included, consistent with prior research24-26: volume (measured as the log of the mean number of VLBW admissions) and level according to VON clas- sification (A: restriction on ventilation, no surgery; B: major surgery; and C: cardiac surgery, corresponding to high level II and level III units in the American Academy of Pediatrics clas- sification). Hospital characteristics to describe the sample were derived from the American Hospital Association Annual Sur- vey of Hospitals.27,28

DATA ANALYSIS

We estimated a logistic regression of infection on understaff- ing in each year, controlling for risk adjusters and NICU-level covariates. We estimated random-effect models by the maxi- mum likelihood method, which adjusted for clustering of in- fants within hospitals. Predicted values were generated from these regressions. Interrater reliability was computed using the Kappa statistic. Estimations were performed in Stata version 10.1 (StataCorp), with a P value of .05 in 2-tailed tests.

Table 2. Characteristics of the NICUs and Infants

Variable

No. (%)

2008 2009

NICUs No. of NICUs 67 67 NICU levels

A 7 (10) 9 (13) B 41 (61) 40 (60) C 19 (28) 18 (27)

Annual volume of VLBW admissions, mean (SD) 108 (63) 105 (64) VLBW infants (eligible for nosocomial infection)

No. of VBLW infants 5713 5558 Nosocomial infection 938 (16.4) 775 (13.9) Birth weight, mean (SD), g 1077 (277) 1072 (278) Gestational age, mean (SD), wk 28.4 (2.8) 28.4 (2.8) 1-min Apgar score, mean (SD) 5.5 (2.5) 5.4 (2.4) Small for gestational age 1134 (19.9) 1118 (20.1) Multiple birth 1701 (29.8) 1600 (28.8) Congenital malformation 200 (3.5) 209 (3.8) Vaginal delivery 1631 (28.5) 1526 (27.5) Had prenatal care 5468 (95.7) 5341 (96.1) Male 2878 (50.4) 2770 (49.8) Race/ethnicity, %

Non-Hispanic white 2905 (50.8) 2757 (49.6) Non-Hispanic black 1641 (28.7) 1702 (30.6) Othera 1167 (20.4) 1099 (19.8)

Abbreviations: NICU, neonatal intensive care unit; VLBW, very low birth weight. aAll other races/ethnicities, including Hispanic.

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RESULTS

HOSPITAL AND INFANT CHARACTERISTICS

Our sample comprised mostly higher level NICUs (87% were levels B and C) compared with the VON (66% were levels B and C and 34% were level A). Compared with the universe of US hospitals with a NICU, our sample con- tained more teaching hospitals (26% in the United States vs 51% in the study sample) and somewhat more not-for- profit hospitals (71% in the United States vs 85%), as well as larger units (a mean of 22 beds in the United States vs 33). Many of the participating hospitals had achieved rec- ognition for nursing excellence through Magnet accredi- tation (40% vs 19% in the United States).29

Infants in our sample had mean birth weights of 1077 g in 2008 and 1072 g in 2009, as well as a mean gesta- tional age of 28.4 weeks in both years. The racial and eth- nic composition of the sample was approximately half non-Hispanic white, 30% non-Hispanic black, and 20% other (Table 2).

INFECTION RATES

The percentages of VLBW infants with hospital- associated infection were 16.4% in 2008 and 13.9% in 2009. This decline was consistent with a secular trend in nosocomial infections among VLBW infants, as re- ported by Horbar and colleagues.30 The infection rates ranged from the 25th percentile of 10.0% in 2008 and 8.8% in 2009 to the 75th percentile of 20.3% in 2008 and 16.4% in 2009.

INFANT ACUITY DEFINITIONS

The infant acuity definitions developed for neonatal in- tensive care nursing are listed in Table 1. The defini- tions specify feeding, ventilation, medication, monitor- ing, and other differences across acuity levels. The classification had high interrater reliability (� = 0.79). In 2009, there were few infants in the 2 highest acuity lev-

els (8%), with most in the 2 lowest levels (66%). The pro- portions of the highest acuity infants were slightly greater in 2008 (12%).

COMPLIANCE WITH GUIDELINES

On average, each infant had 0.4 of a nurse (in the 2008 data, 4046 nurses were assigned to 10 394 infants; in the 2009-2010 data, 3645 nurses were assigned to 8804 in- fants). Relative to the guidelines, on average, hospitals understaffed 47% of all NICU infants in 2008 and 31% in 2009 (Table 3). Hospitals understaffed 80% of high- acuity infants (levels 4 and 5) in 2008 and 68% in 2009. Higher infant acuity was associated with more under- staffing. For example, in 2009, 20% of acuity level 1 in- fants and 68% of high-acuity infants (levels 4 and 5) were understaffed. To meet guidelines, an additional 0.11 of a nurse per infant overall and an additional 0.34 of a nurse per high acuity infant (ie, levels 4 and 5) would have been needed in 2009. In 2008, the understaffing was higher. There was very little overstaffing. Hospitals overstaffed 4% and 6% of their infants in 2008 and 2009, respec- tively. The overstaffing provided a very small offset (0.01 and 0.02 of nurse per infant in 2008 and 2009, respec- tively) to counterbalance understaffing.

In 2009, 55% of units understaffed at least 25% of their infants and 16% understaffed at least 50% of their in- fants. Five units had no understaffing in 2009.

MULTIVARIATE REGRESSION RESULTS

As shown in Table 4, a 1 standard deviation increase in the amount of a nurse per infant needed to meet guide- lines (0.11 of a nurse in 2008 and 0.08 of a nurse in 2009) was associated with higher odds of infection in 2008 (ad- justed odds ratio, 1.39; 95% CI, 1.19-1.62; P � .001) and 2009 (adjusted odds ratio, 1.40; 95% CI, 1.19-1.65; P � .001).

The odds ratios for understaffing translate into pre- dicted infection rates as displayed in the Figure. This represents the predicted risk for infection associated with

Table 3. Recommended Staffing Ratios, Infant Acuity Distribution, and Nurse Understaffing Relative to Guidelines3,4

Mean (SD)a

Overall

Acuity Level

1 2 3 4 5

Recommended nurse to patient ratios according to guidelines NA 1:3-4 1:2-3 1:1-2 1:1 �1:1 Infants by acuity level, %

2008 100 32 28 28 8 4 2009 100 33 33 26 6 2

Infants who were understaffed, % 2008 47 (20) 34 (21) 46 (22) 53 (23) 89 (15) 63 (30) 2009 31 (19) 20 (19) 29 (21) 37 (26) 77 (33) 42 (40)

Fraction of a nurse/patient needed to achieve minimum recommended nurse to patient ratio

2008 .19 (.11) .10 (.08) .15 (.09) .23 (.11) .52 (.19) .37 (.24) 2009 .11 (.08) .04 (.05) .07 (.06) .13 (.10) .39 (.22) .20 (.22)

Abbreviation: NA, not available. aStatistics were calculated from 4046 nurses assigned to 10 394 infants in 2008 and 3645 nurses assigned to 8804 infants in 2009-2010.

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understaffing for an infant who had average infection risk, based on estimates from the random-effects logit model. In a unit with no understaffing, the predicted infection rate was 9%. At the 2009 median understaffing level (0.11 of a nurse per infant), the predicted infection rate was 14%. At the 90th percentile of understaffing (0.22 of a nurse per infant), the infection rate was 21%.

COMMENT

The NICU provides care for critically ill infants and is a highly nurse-intensive setting. Yet, little is known about the adequacy of nurse staffing in US NICUs or the potential implications of understaffing for infant out- comes. Our results document widespread understaffing relative to guidelines: one-third of NICU infants were understaffed. Understaffing varies further across acuity levels, with the greatest fraction of understaffed infants (68% in 2009) requiring the most complex critical care

(acuity levels 4 and 5). An additional tenth of a nurse per infant would be needed on average to meet current national guidelines; however, for the high-acuity infants, an additional third of a nurse per infant would be needed. This translates into a 25% increase in nurse staffing on average (ie, to increase from observed staff- ing of 0.4 of a nurse per infant by an additional 0.11 of a nurse per infant) or an additional nurse for every 9 infants. These are conservative estimates of understaff- ing because the measures are based on the guideline minimums.

The widespread understaffing is noteworthy in a hos- pital sample thatwasdisproportionately recognized fornurs- ing excellence. The overall registered nurse staffing in sample hospitals was higher than in US hospitals with a NICU (10.4 vs 9.4 hours/patient day; P � .05; authors’ cal- culations from American Hospital Association data). Staff- ing levels in all US NICUs may be lower than those ob- served here. Sample NICUs may have better-trained nurses than other hospitals and this training composition may in- fluence nurse staffing. However, the guidelines indicate that a specialized staff is the minimum expectation.

In VLBW infants, NICU nurse understaffing relative to guidelines was associated with a sizable increase in in- fection risk. A 1 standard deviation–higher amount of nurse understaffing per infant (ie, one-tenth of a nurse) was associated with 40% higher odds of infection. There are wide variations in infection rates across units, dem- onstrating that low infection rates are achievable: 9% of units in 2009 had infection rates below 5%. Quality im- provement initiatives have been successful in reducing rates of infection in the NICU31-34 and in other set- tings.34-36 With a median length of stay in the NICU of 62 days (in the 2009 VON) for VLBW infants, exposure to understaffing should be minimized to reduce infec- tion risk. The NICU caseload is heavily concentrated in the care of VLBW infants. In a subset of 30 hospitals with VON data on all infants, VLBW infants accounted for 1 in 5 admissions but half of patient days.

Very low-birth-weight infants are a high-risk popu- lation, accounting for half of infant deaths in the United States each year.16 Their NICU stays are among the most expensive hospitalizations.1 Hospital-associated infec- tions are associated with higher mortality and costs for these vulnerable infants. The development of an infec- tion more than doubles the mortality rate among VLBW infants.20 In VON, among VLBW infants who survived 3 days, 13.8% of those with nosocomial infection died com- pared with 5.5% without infection. Very low-birth- weight infants who develop an infection have lengths of stay that are 4 to 7 days longer than those without, ad- justed for infant risk.21

Medicaid is a principal payer for the hospital care of 42% of preterm and low-birth-weight infants.23 The Cen- ter for Medicare and Medicaid Innovation was recently formed under the Affordable Care Act to foster value in health care through health systems and payment inno- vations. The Centers for Medicare and Medicaid Ser- vices has already focused on hospital-associated infec- tion in its payment systems. Medicaid will no longer reimburse the additional hospital costs associated with vascular catheter-associated infection. For hospitals to

Table 4. Risk for VLBW Infant Infection Associated With Nurse Understaffing and NICU Variables

Odds Ratio (95% CI)a

2008 2009

Understaffing amountb

1.39 (1.19-1.62) 1.40 (1.19-1.65)

NICU level A 1.33 (0.65-2.70) 1.52 (0.84-2.75) B 0.69 (0.50-0.96) 1.02 (0.70-1.48) C 1 [Reference] 1 [Reference]

Natural log of annual volume of VLBW admissions

0.82 (0.61-1.09) 0.82 (0.63-1.07)

Abbreviations: NICU, neonatal intensive care unit; VLBW, very low birth weight.

aOdds ratios and CIs were derived from random-effects logistic regression models. The 2008 model had 5713 observations; the 2009 model had 5558 observations. Infant risk adjusters were gestational age, gestational age squared, 1-minute Apgar score, small for gestational age, multiple birth, congenital malformation, vaginal delivery, prenatal care, race/ethnicity, and sex.

bFraction of a nurse per patient needed to achieve the minimum recommended nurse to patient ratio.

0.00 0.00 0.10 0.20 0.300.15 0.25 0.35 0.40

0.30

0.25

In fe

ct io

n Ra

te

Understaffing Amount (Fraction of a Nurse per Patient)

0.20

0.15

0.10

0.05

0.05

Figure. Predicted risk-adjusted infection rates by nursing unit understaffing amount.

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respond effectively to these incentives, they require in- formation on such factors as adequate nurse staffing. Pre- viously, for nurse staffing, definitions for the national guidelines in NICUs that have existed since 1992 were not available. Definitions that have high interrater reli- ability are now available to guide such efforts. The guide- lines can be reevaluated now that a reliable acuity clas- sification is available.

In the decade since Crossing the Quality Chasm,37 there have been numerous calls to improve the quality of the health care system. Improving the quality of care for VLBW infants was emphasized in the Institute of Medi- cine report on preterm birth,1 which called for better mea- surement of the quality of care in NICUs and pointed to nurse staffing as a promising avenue for developing such measures. The focus on infants was reinforced by the re- cent March of Dimes volume, Towards Improving the Out- comes of Pregnancy III.38 Our results demonstrate a siz- able gap in the quality of care for these infants.

Our study had limitations. The VON hospitals do not fully represent all US hospitals with a NICU and our sample was disproportionately recognized for nursing excel- lence. The cross-sectional research design prevented causal inferences. The analyses presented here do not take into consideration other factors that may be important in NICU staffing decisions such as nonnursing personnel.

In conclusion, our findings suggest that the most vul- nerable hospitalized patients, unstable newborns requir- ing complex critical care, do not receive recommended levels of nursing care. Even in some of the nation’s best NICUs, nurse staffing does not match guidelines. Hos- pital administrators and NICU managers must assess their staffing decisions to devote needed nursing care to criti- cally ill infants.

Accepted for Publication: December 13, 2012. Published Online: March 18, 2013. doi:10.1001 /jamapediatrics.2013.18 Author Affiliations: Department of Health Systems and Policy, School of Public Health, University of Medicine and Dentistry of New Jersey, Piscataway, New Jersey (Dr Rogowski); Department of Economics, Dartmouth Col- lege, Hanover, New Hampshire, and National Bureau of Economic Research, Cambridge, Massachusetts (Dr Staiger); College of Nursing, Ohio State University, Co- lumbus, Ohio (Dr Patrick); Department of Pediatrics, Uni- versity of Vermont (Mr Kenny), Vermont Oxford Net- work (Dr Horbar), Burlington, Vermont; and Center for Health Outcomes and Policy Research, School of Nurs- ing, Department of Sociology, Leonard Davis Institute of Health Economics, University of Pennsylvania, Philadel- phia (Dr Lake). Correspondence: Jeannette A. Rogowski, PhD, Depart- ment of Health Systems and Policy, School of Public Health, University of Medicine and Dentistry of New Jer- sey, 683 Hoes Lane W, Piscataway, NJ 08854 (rogowsje @umdnj.edu). Author Contributions: Study concept and design: Rogowski, Staiger, Patrick, Horbar, and Lake. Acquisi- tion of data: Rogowski, Patrick, Horbar, Kenny, and Lake. Analysis and interpretation of data: All authors. Drafting of the manuscript: Rogowski, Staiger, Patrick, Horbar, and

Lake. Critical revision of the manuscript for important in- tellectual content: All authors. Statistical analysis: Rogowski, Staiger, and Kenny. Obtained funding: Rogowski, Staiger, Patrick, and Lake. Administrative, technical, and mate- rial support: Rogowski and Lake. Study supervision: Rogowski, Horbar, and Lake. Conflict of Interest Disclosures: Dr Staiger holds an eq- uity interest in ArborMetrix Inc, a company that sells ef- ficiency measurement systems and consulting services to insurers and hospitals. Dr Horbar is an employee of the Vermont Oxford Network, for which he serves as the chief executive and scientific officer. Funding/Support: This research was funded by grant R01NR010357 from the National Institute of Nursing Re- search and support from the Robert Wood Johnson Foun- dationInterdisciplinaryNursingQualityResearchInitiative. Disclaimer: The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institute of Nursing Research or the National Institutes of Health.

REFERENCES

1. Institute of Medicine. Preterm Birth: Causes, Consequences, and Prevention. Wash- ington, DC: The National Academies Press; 2006.

2. American Academy of Pediatrics, American College of Obstetricians and Gyne- cologists. Inpatient perinatal care services. In: Freeman RK, Poland RL, eds. Guide- lines for Perinatal Care. 3rd ed. Washington, DC: American Academy of Pediat- rics and American College of Obstetricians and Gynecologists; 1992.

3. American Academy of Pediatrics, American College of Obstetricians and Gyne- cologists. Inpatient perinatal care services. In: Lemons JA, Lockwood CJ, eds. Guidelines for Perinatal Care. 6th ed. Washington, DC: American Academy of Pe- diatrics and American College of Obstetricians and Gynecologists; 2007.

4. Association of Women’s Health Obstetric and Neonatal Nurses. Guidelines for Professional Registered Nurse Staffing for Perinatal Units. Washington, DC: As- sociation of Women’s Health Obstetric and Neonatal Nurses; 2010.

5. 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(7):937-944.

6. Penoyer DA. Nurse staffing and patient outcomes in critical care: a concise review. Crit Care Med. 2010;38(7):1521-1528, quiz 1529.

7. Kilbride HW, Wirtschafter DD, Powers RJ, Sheehan MB. Implementation of evidence- based potentially better practices to decrease nosocomial infections. Pediatrics. 2003;111(4, pt 2):e519-e533.

8. McCourt M. At risk for infection: the very-low-birth-weight infant. J Perinat Neo- natal Nurs. 1994;7(4):52-64.

9. Cimiotti JP, Haas J, Saiman L, Larson EL. Impact of staffing on bloodstream in- fections in the neonatal intensive care unit. Arch Pediatr Adolesc Med. 2006; 160(8):832-836.

10. Andersen BM, Lindemann R, Bergh K, et al. Spread of methicillin-resistant Staphy- lococcus aureus in a neonatal intensive unit associated with understaffing, over- crowding and mixing of patients. J Hosp Infect. 2002;50(1):18-24.

11. Haley RW, Cushion NB, Tenover FC, et al. Eradication of endemic methicillin- resistant Staphylococcus aureus infections from a neonatal intensive care unit. J Infect Dis. 1995;171(3):614-624.

12. Haley RW, Bregman DA. The role of understaffing and overcrowding in recur- rent outbreaks of staphylococcal infection in a neonatal special-care unit. J In- fect Dis. 1982;145(6):875-885.

13. Harbarth SSP, Sudre P, Dharan S, Cadenas M, Pittet D. Outbreak of Enterobac- ter cloacae related to understaffing, overcrowding, and poor hygiene practices. Infect Control Hosp Epidemiol. 1999;20(9):598-603.

14. Tucker J; UK Neonatal Staffing Study Group. Patient volume, staffing, and workload in relation to risk-adjusted outcomes in a random stratified sample of UK neonatal intensive care units: a prospective evaluation. Lancet. 2002;359(9301):99-107.

15. Pillay T, Nightingale P, Owen S, Kirby D, Spencer A. Neonatal nurse staffing and delivery of clinical care in the SSBC Newborn Network. Arch Dis Child Fetal Neo- natal Ed. 2012;97(3):f174-f178.

16. Mathews TJ, Miniño AM, Osterman MJ, Strobino DM, Guyer B. Annual sum- mary of vital statistics: 2008. Pediatrics. 2011;127(1):146-157.

17. Lewis D, Wilson C. Developmental immunology and role of host defense in fetal

JAMA PEDIATR/ VOL 167 (NO. 5), MAY 2013 WWW.JAMAPEDS.COM 449

©2013 American Medical Association. All rights reserved.

Downloaded From: http://archpedi.jamanetwork.com/ by Jennifer Grossner on 09/28/2015

and neonatal susceptibility to infection. In: Remington JSKJ, Wilson CB, Baker CJ, eds. Infectious Diseases of the Fetus and Newborn Infant. 6th ed. Philadel- phia, PA: The WB Saunders Co; 2006:88-199.

18. Cartlidge P. The epidermal barrier. Semin Neonatol. 2000;5(4):273-280. 19. Ziegler EE, Carlson SJ. Early nutrition of very low birth weight infants. J Matern

Fetal Neonatal Med. 2009;22(3):191-197. 20. Stoll BJ, Hansen N, Fanaroff AA, et al. Late-onset sepsis in very low birth weight

neonates: the experience of the NICHD Neonatal Research Network. Pediatrics. 2002;110(2, pt 1):285-291.

21. Payne NR, Carpenter JH, Badger GJ, Horbar JD, Rogowski J. Marginal increase in cost and excess length of stay associated with nosocomial bloodstream infections in surviving very low birth weight infants. Pediatrics. 2004;114(2):348-355.

22. Stoll BJ, Hansen NI, Adams-Chapman I, et al; National Institute of Child Health and Human Development Neonatal Research Network. Neurodevelopmental and growth impairment among extremely low-birth-weight infants with neonatal infection. JAMA. 2004;292(19):2357-2365.

23. Russell RB, Green NS, Steiner CA, et al. Cost of hospitalization for preterm and low birth weight infants in the United States. Pediatrics. 2007;120(1):e1-e9.

24. Rogowski JA, Horbar JD, Staiger DO, Kenny M, Carpenter J, Geppert J. Indirect vs direct hospital quality indicators for very low-birth-weight infants. JAMA. 2004; 291(2):202-209.

25. Chung JH, Phibbs CS, Boscardin WJ, et al. Examining the effect of hospital-level factors on mortality of very low birth weight infants using multilevel modeling. J Perinatol. 2011;31(12):770-775.

26. Phibbs CS, Baker LC, Caughey AB, Danielsen B, Schmitt SK, Phibbs RH. Level and volume of neonatal intensive care and mortality in very-low-birth-weight infants. N Engl J Med. 2007;356(21):2165-2175.

27. American Hospital Association. AHA Annual Survey Database, 2008 edition. Chi- cago, IL: American Hospital Association.

28. American Hospital Association. AHA Annual Survey Database, 2009 edition. Chi- cago, IL: American Hospital Association.

29. American Nurses Credentialing Center. Health care organizations with Magnet- recognized nursing services. http://www.nursecredentialing.org/Magnet /FindAMagnetFacility.aspx. Accessed March 29, 2012.

30. Horbar JD, Carpenter JH, Badger GJ, et al. Mortality and neonatal morbidity among infants 501 to 1500 grams from 2000 to 2009. Pediatrics. 2012;129(6):1019- 1026.

31. Payne NR, Barry J, Berg W, et al; Stop Transmission of Pathogens (STOP) Team of the St. Paul Campus; Prevent Infection Team (PIT) of the Minneapolis Cam- pus of Children’s Hospitals and Clinics of Minnesota. Sustained reduction in neo- natal nosocomial infections through quality improvement efforts. Pediatrics. 2012; 129(1):e165-e173.

32. Wirtschafter DDPR, Powers RJ, Pettit JS, et al. Nosocomial infection reduction in VLBW infants with a statewide quality-improvement model. Pediatrics. 2011; 127(3):419-426.

33. Jacob JSD, Sims D, Van de Rostyne C, Schmidt G, O’Leary K. Toward the elimi- nation of catheter-related bloodstream infections in a newborn intensive care unit (NICU). Jt Comm J Qual Patient Saf. 2011;37(5):211-216, 193.

34. Kaplan HC, Lannon C, Walsh MC, Donovan EF; Ohio Perinatal Quality Collabora- tive. Ohio statewide quality-improvement collaborative to reduce late-onset sep- sis in preterm infants. Pediatrics. 2011;127(3):427-435.

35. Miller MR, Griswold M, Harris JM II, et al. Decreasing PICU catheter-associated bloodstream infections: NACHRI’s quality transformation efforts. Pediatrics. 2010; 125(2):206-213.

36. Pronovost P, Needham D, Berenholtz S, et al. An intervention to decrease catheter- related bloodstream infections in the ICU. N Engl J Med. 2006;355(26):2725-2732.

37. Institute of Medicine. Crossing the Quality Chasm: A New Health System for the 21st Century. Washington, DC: National Academy Press; 2001.

38. March of Dimes. Towards Improving the Outcome of Pregnancy III: Enhancing Perinatal Health Through Quality, Safety and Performance Initiatives. White Plains, NY: March of Dimes.

Poetry in Pediatrics

The Reason I Am

I have forgotten the pain I have forgotten the wounds The pain of unsleeping nights The wounds of failed exams; I am a physician now I am the patients’ hope Their teardrops move me. I became a reason for the suffering children I became a champion for my friends A strange, tired but amazing child for my parents An eternal busy mother And, for sure, a hard-to-understand wife. All of these because I chose to be a physician, And I swore to be skilled in my job Because I like my career, I like children And I want to bring them back to health. Please, forgive me for my neglect Try to understand and let me be forthright And I promise to be A real mother, although eternally busy A real wife, although sometimes hard to understand A good, but strange, child for my parents And also, a champion physician.

Simona Gurzu, MD, PhD

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