J Paediatrics Child Health - 2019 - Ahearn

doi:10.1111/jpc.
14580
ORIGINAL ARTICLE
Impact of inhaled nitric oxide stewardship programme in a

neonatal intensive care unit
Joshua Ahearn ,1 Malavika Panda,2 Hazel Carlisle1,2 and Tejasvi Chaudhari1,2
1
Australian National University Medical School, Canberra and 2Department of Neonatology, Centenary Hospital for Women and Children, Canberra
Hospital, Woden, Australian Capital Territory, Australia
Aim: Inhaled nitric oxide (iNO) is the most common, although expensive, therapy for persistent pulmonary hypertension of the newborn and
hypoxaemic respiratory failure. With significant variation in iNO delivery practices amongst clinicians, this study aimed to assess the effectiveness
of a stewardship programme in increasing clinician compliance with revised, standardised protocols and to measure the impact of compliance on
iNO therapy use.
Methods: Initiation and weaning protocols for iNO were introduced to the neonatal intensive care unit at The Centenary Hospital on 01 March
2016. A 2-year stewardship programme was utilised to assess protocol compliance and the resulting iNO usage impacts were measured. A com-
bined retrospective and prospective study from 1 March 2014 to 28 February 2018 was conducted to compare the patterns of iNO utilisation
between the pre- and post-stewardship cohorts.
Results: The pre-stewardship cohort incorporated 18 neonates, receiving 19 iNO treatment episodes, and 18 neonates, receiving 21 iNO treat-
ment episodes, in the post-stewardship cohort. No significant difference in patient demographics was determined. Compliance with the protocols
improved from 61% in year 1 to 88% in year 2 of the stewardship programme. Significant reductions were observed in median total hours of iNO
therapy per patient (P = 0.0014) and in median time from therapy initiation to initial wean (P < 0.0001). The cost of iNO therapy reduced 52% dur-
ing the stewardship programme with no increase in adverse patient outcomes.
Conclusion: An iNO stewardship programme could be safely implemented in any NICU leading to increased protocol compliance with a benefi-
cial reduction in iNO usage and cost.
Key words: inhaled nitric oxide; persistent pulmonary hypertension of newborn; stewardship programme.
What is already known on this topic What this paper adds

1 Inhaled nitric oxide (iNO) elicits a safe, powerful pulmonary 1 The introduction of a stewardship programme for iNO use within
vasodilatory effect in the treatment of persistent pulmonary a neonatal intensive care unit resulted in increased compliance
hypertension of the newborn and hypoxaemic respiratory failure with the prescribed protocol.
when administered correctly. 2 Increased protocol compliance led to a safe and clinically justifi-
2 Published protocol guidelines are attributed as a key component able reduction in medication exposure. This reduced iNO costs
in the reduction of practice variation and in the quality improve- within the unit by 52%.
ment of health care.
3 Stewardship programmes enable the effective monitoring of cli-
nician compliance with protocols, thereby improving the capac-
ity of services to deliver safe and efficient health care.
During fetal life, lungs are filled with fluid, pulmonary vascular resis- decreased PVR and increased systemic vascular resistance (SVR).
tance (PVR) is high and pulmonary blood flow is diminished. After Conditions that interfere with the normal post-natal decline in
birth and following aeration of the lungs, the organ of gas exchange PVR/SVR ratio can cause the fetal circulation to persist and could
transitions from the placenta to the lungs. This is accompanied by result in persistent pulmonary hypertension of newborn (PPHN).1
PPHN is a serious neonatal emergency that can result in hypoxaemic
respiratory failure (HRF) and death.2 It is characterised by increased
Correspondence: Dr Tejasvi Chaudhari, Department of Neonatology, PVR, intrapulmonary shunting with resultant ventilation-perfusion
Centenary Hospital for Women and Children, Canberra Hospital, PO Box
(V/Q) mismatch, right-to-left extrapulmonary shunting through the
11, Woden, ACT 2606, Australia. Fax: +61 26244 3422; email: tejasvi.
chaudhari@act.gov.au
ductus arteriosus and foramen ovale, progressively leading to arterial
hypoxaemia.3 PPHN can be one of three types: (i) primary or idio-
Conflict of interest: None declared. pathic due to remodelled pulmonary vasculature but normal paren-
Accepted for publication 16 July 2019. chyma; (ii) abnormal pulmonary vasoconstriction following perinatal
Journal of Paediatrics and Child Health 56 (2020) 265–271 265

© 2019 Paediatrics and Child Health Division (The Royal Australasian College of Physicians)
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Inhaled nitric oxide stewardship J Ahearn et al.
asphyxia or parenchymal lung disease such as hyaline membrane This group developed a working stewardship programme which
disease, pneumonia, meconium aspiration; or (iii) hypoplastic vascu- was implemented within the NICU on 1 March 2016. The proto-
lature as seen in pulmonary hypoplasia associated with congenital col evidence review had focussed on indications for use, response
diaphragmatic hernia.1,2,4 to therapy and weaning procedures whilst seeking to maintain
Treatment of PPHN relies on supportive treatment such as oxy- patient safety, minimise practice variations and ensure efficient
gen administration, in addition to effective lung recruitment utilisation of the expensive resource.
using CPAP or ventilation. In severe cases, selective dilation of Evidence review and protocol development led to revised iNO
the pulmonary vasculature may be necessary.3 Endogenous nitric initiation and weaning practices within the NICU, as shown in Fig-
oxide (NO) regulates vascular tone by activating guanylate ures 1 and 2. These protocols promote nurse-led care with the bed-
cyclase leading to production of cyclic guanosine monophosphate side nurse authorised to wean iNO within set protocol limits. Key
and subsequent smooth muscle relaxation.3,5,6 Exogenous iNO is criteria for iNO initiation were: (i) clinical diagnosis of HRF with cli-
a selective pulmonary vasodilator that acts by decreasing the pul- nician performed ultrasound (CPU) confirmation of PPHN;
monary artery pressure without any effect on systemic artery (ii) oxygenation index (OI) of ≥15 – consideration of iNO; OI ≥20 –
pressure resulting in decreased PVR:SVR ratio.4,7 Oxygenation iNO recommended; (iii) ventilation optimised and confirmed
improves as previously constricted vessels dilate in well- through recent imaging; and (iv) detailed response and non-
ventilated areas of the lung, thereby reducing the occurrence of response to therapy indicators to guide iNO treatment, as per
intrapulmonary shunting and V/Q mismatch.5,8 Figures 1 and 2.9 Availability of repeat CPU is inconsistent therefore
A review of iNO usage within the neonatal intensive care unit ultrasound evidence of improvement was not mandatory and as
(NICU) at The Centenary Hospital for Women and Children in Can- such not required prior to weaning. The revised weaning guidelines
berra revealed increased usage from 2014 (442 h) to 2015 (928 h). detailed the sequence of iNO concentrations, time between weaning
Detailed review revealed significant clinician variation with regard increments and the weaning failure criteria and considerations.
to the initiation of iNO, weaning thresholds, and rates and timing of Visual flow charts for these guidelines were distributed
weaning. This was attributed to lack of standardised iNO usage prac- amongst the NICU staff with education conducted prior to
tices. Junior staff lacked the authority or confidence to make stewardship commencement. On initiation of iNO therapy
weaning decisions, often waiting for morning rounds and more throughout the stewardship programme visual charts were
senior staff presence before weaning was commenced. This is com- displayed beside each patient to facilitate compliance with the
monly observed across similar units.9,10 iNO is expensive, with an protocol.
hourly rate of 138.5AUD in Australia (previously this was charged Compliance with the protocol was assessed as: doses and dura-
at a fixed price per patient use). Prolonged use of iNO due to variation of therapy were within the specified parameters; and evi-
tion in practice without clinical justification has significant financial dence of weaning criteria failure with the subsequent reversion
repercussions both to the hospital and health-care system.11 to previous dosage documented. Non-compliance was assessed as
Although adverse effects are rare at the current iNO starting failure to wean or cease therapy when protocol indicators for
dose of 20 parts per million (ppm), prolonged usage has risks.12 dose reduction or discontinuation were met. Each individual
Adverse effects of iNO may result from its direct inhibitory effects opportunity for compliance within a treatment episode of iNO
on platelet function resulting in significant bleeding, or through was assessed.
its formation of reactive products, namely methemoglobin and Throughout the duration of the post-stewardship cohort, regu-
nitrogen dioxide; both of these products are actively monitored lar reviews were conducted by the Stewardship team to monitor
during iNO therapy.13–15 The risk of adverse effect occurrence protocol compliance rates and, had it been required, initiate addi-
necessitates that iNO be delivered at the lowest effective dose tional protocol revisions. The initiation of therapy and weaning
possible for as short a duration as possible. protocols that were monitored for compliance throughout this
Stewardship programmes are targeted interventions that seek study are still utilised within the NICU post stewardship comple-
to improve protocol adherence, minimise variations and unneces- tion on 28 February 2018.
sary resource expenditure whilst promoting better, safer practices
that maximise patient outcomes.11 This study aimed to determine
compliance with the unit’s revised, evidence-based standardised Study design
protocols, which promote nurse-led care, through utilisation of a
stewardship programme, and to report on resulting impacts on A combined prospective and retrospective cohort study was con-
iNO therapy use in the NICU setting. The goal of increased proto- ducted utilising a deidentified data set. The Research Ethics and Gov-
col compliance is to reduce the risk of patient harm by safely ernance Office of the Australian Capital Territory Heath Department
reducing iNO use and therefore unnecessary department costs.11 approved this study as a quality assurance project (ETHR.17.212);
thereby, parental consent was not required. Study inclusion criteria
were all neonates who received iNO, initiated at the NICU or on
Methods retrieval, during the study period 01 March 2014 to 28 February
2018. The study period was divided into a pre-stewardship cohort
Stewardship and guideline development process
(1 March 2014 to 29 February 2016) and a post-stewardship cohort
Following review of available evidence regarding indications for (1 March 2016 to 28 February 2018). Therapy was initiated on con-
iNO usage and the development of an agreed treatment protocol firmation of PPHN by attending physician utilising CPU or confirma-
in January 2016, a clinical meeting was convened consisting of tion via echocardiography by cardiologist, following clinical diagnosis
neonatologists, the nurse leadership group and NICU fellows. of HRF.
266 Journal of Paediatrics and Child Health 56 (2020) 265–271

J Ahearn et al. Inhaled nitric oxide stewardship
Fig. 1 Inhaled nitric oxide initiation protocol. ABG, arterial-blood gas; CXR, chest X-ray; ECHO, echocardiogram; iNO, inhaled nitric oxide; MAP, mean arte-
rial pressure; OI, oxygenation index; ppm, parts per million.

J Ahearn et al.
Journal of Paediatrics and Child Health 56 (2020) 265–271
Fig. 2 Inhaled nitric oxide weaning protocol. iNO, inhaled nitric oxide; ppm, parts per million.
Inhaled nitric oxide stewardship
268
Data extraction and analysis

Table 1 Patient demographics
Neonates were identified for the pre-stewardship cohort
Pre- Post-
through iNO usage reporting from the Hospital’s Technical
stewardship stewardship P value†
Division. Patient data were retrieved using the ACT Health
electronic record system. Data obtained for each patient Treatment episodes of iNO, n 19 21 NA
included sex, gestational age and weights at initiation of iNO Patients, n 18 18 NA
therapy, clinical diagnosis for iNO initiation, conduct of treat- Sex, M/F, n 11/7 9/9 0.491
ment and patient outcome including adverse events, extracor- Body weight at initiation 2086 2580 0.968
poreal membrane oxygenation (ECMO) referral or death. of iNO, g, median (IQR) (1510–3176) (1027–3533)
Post-stewardship cohort data was collected via the dedicated Gestational age at initiation 33 (30–37) 35 (27–38) 0.968
stewardship form by the patient’s treating nurse, with addi- of iNO in completed weeks,
tional data obtained via records as required. The time from median (IQR)
initiation of therapy to first wean and total duration of iNO Death, n 4 2 0.803
therapy was calculated to the nearest hour via the use of ECMO, n 0 0 NA
observation charts, which detailed the time at which ventila- Alternative vasodilators used, n 18 15 0.053
tion equipment settings were changed in addition to the con- †Mann–Whitney U-test and χ2 test were used for continuous and cate-
centration of iNO delivered. gorical data, respectively. P value <0.05 was considered significant.
The data were compiled and transcribed into deidentified ECMO, extracorporeal membrane oxygenation; iNO, inhaled nitric
tables, enabling statistical analysis. Continuous data were com- oxide; IQR, interquartile range; NA, not applicable.
pared using Mann–Whitney U-test, and categorical data were
compared using χ2 test. Statistical software used was IBM SPSS
(version 25, an IBM company, Chicago, IL, USA). Data will be
presented as number and percentage or median and interquartile therapy was 79 and 86% in the pre- and post-stewardship
ranges. A P value of <0.05 was considered statistically significant. cohorts, respectively, with no significant variation in patient out-
come (P = 0.574). No significant variation in the administration
of alternative pulmonary vasodilators (sildenafil, milrinone and
Results alprostadil) prior to, during or following the iNO treatment was
observed.
Following stewardship implementation, compliance with the new
The analysis between cohorts of iNO utilisation within the
protocols was measured at the end of both the first and second
NICU by total time, time per patient, time to first wean and time
year, with compliance increasing from 61% in the first year to
from first wean to withdrawal are shown in Table 2. This analysis
88% in the second year. Prior to the establishment of the stew-
of weaning times included 19 pre-stewardship treatment episodes
ardship programme, significant variation in the weaning of iNO
(95%) and 21 post-stewardship treatment episodes (88%).
was observed within the NICU.
Comparison between the two cohorts displayed a significant
Total iNO therapy duration was decreased from 1595 h (n = 20
decrease in the total hours of iNO administered, from a median
treatment episodes) pre-stewardship (March 2014 to February
of 67.9 h/iNO treatment episode (41.7–94.8) pre-stewardship to
2016) to 774 h (n = 24 treatment episodes) post-stewardship
33.5 h/iNO treatment episode (27.0–40.3) post-stewardship
(March 2016 to February 2018). In the pre-stewardship cohort,
(P = 0.0014). A significant reduction in median time to wean
18 patients received a total of 20 treatment episodes of iNO, com-
from iNO initiation to first wean in the post-stewardship cohort
pared with 21 patients receiving a total of 24 iNO treatment epi-
was also shown (P < 0.0001). No significant decrease was
sodes in the post-stewardship cohort. Of these patients, three
observed in time from first wean to discontinuation of iNO.
were excluded due to withdrawal of care or death and one
Under current iNO costing practices, the total price of iNO
excluded due to discontinuation of iNO for transfer to a quater-
therapy was reduced from $220 907 to $107 199 in the post-
nary hospital for escalation of care. One treatment episode was
stewardship period (calculated hourly cost). This equated to a
excluded from the pre-stewardship cohort with three excluded
52% cost reduction.
from the post-stewardship cohort.
Table 1 shows that there were no significant differences in the
patient characteristics or in adverse outcomes such as death or Discussion
ECMO use between the pre- and post-stewardship cohorts. The
median (interquartile range) gestational age in the pre- Despite widespread, high quality evidence informing neonatal iNO
stewardship cohort was 33 weeks (30–37) as compared to use, variations in NICU practices resulted in prolonged and poten-
35 weeks (27–38) in the post-stewardship cohort (P = 0.968). tially harmful medication exposure whilst additionally increasing
The predominant cause of initiating iNO in both cohorts was the economic burden on limited health-care resources.9,10 In
PPHN (89% pre-stewardship and 95% post-stewardship), with response to this, revised evidence-based protocols for the initiation
HRF accounting for the remainder of the patients (11% pre- and weaning of iNO was introduced within the NICU. In support
stewardship and 5% post-stewardship). No patient was initiated of this process, the practice changes were embedded within a
on iNO for a diagnosis other than PPHN, HRF, or both. In all 2-year post-implementation stewardship programme.
instances of iNO therapy initiated within the NICU, no patients Published protocols within health-care settings are attributed
were exposed to a dose greater than 20 ppm. Response to iNO as a key component in the reduction of practice variation and in

Inhaled nitric oxide stewardship J Ahearn et al.
Table 2 Inhaled nitric oxide (iNO) usage within neonatal intensive care unit
Pre-stewardship Post-stewardship P value†
Treatment episodes of iNO given, n 19 21 NA

Hours/course, median (IQR) 67.9 (41.7–94.8) 33.5 (27.0–40.3) 0.0014
Hours from initiation of therapy to first wean, median 38.7 (26.3–63.3) 13.4 (7.3–22.6) <0.0001
(IQR)
Hours from first wean to discontinuation, median (IQR) 12.8 (9.0–27.6) 14.5 (10.9–26.1) 0.789
Oxygenation index prior to commencement of iNO, 26.4 (18.6–36.4) 37.5 (24.6–55.9) 0.207
median (IQR)
Oxygenation Index at first wean, median (IQR) 9.3 (7.1–12.1) 12.7 (5.6–14.5) 0.433
Total cost of iNO, AUD$ 220 907 107 199 NA
†Mann–Whitney U-test and χ2 test were used for continuous and categorical data, respectively. P value <0.05 was considered significant. IQR,
interquartile range; NA, not applicable.
health-care quality improvement; monitoring of protocol compli- patients undergoing treatment and the empowerment to wean
ance determines its effectiveness and helps to monitor safety. iNO by the treating nurse. Changes predominately occurred in
Amir Elmekkawi et al. demonstrated in 2016 that the imple- median time to wean from iNO initiation to first wean, indicating
mentation of a stewardship programme for iNO use in their the greatest variation in iNO therapy practices occurred within
NICU led to increased protocol compliance and a safe reduction the physician group. Following first wean, a shift from physician-
in costs.9 This study provides further evidence in support of led to nurse-led weaning based on set criteria was able to
their findings. enhance protocol compliance.
As previously outlined, prescribed protocol compliance During protocol revision and the development of a stewardship
increased within the post-stewardship cohort, reaching 61% in programme, we found no published guidelines to shape the
the first year and 88% in the second year. Protocol deviation delivery of iNO in premature babies. Consequently, our protocol
during the first year is attributed to either reduced protocol was standardised to a dosage of 20 ppm regardless of gestational
awareness or consultant initiated slow weaning outside the age or weight. This iNO usage practice is supported by clinical tri-
recommended protocol sometimes related to the lack of avail- als showing increased oxygenation without a reduction in mor-
ability of CPU scans. We have hypothesised that this arose from tality in premature babies with HRF.16 This study safely reduced
the use of caution and a hesitation towards the effect of rapid iNO usage rates with no adverse effects from iNO therapy
weaning. observed in the preterm infant cohort.
A detailed comparison was conducted at the 1-year mark to
determine protocol compliance and the initial impact on iNO
Improving quality
use within the NICU. This analysis of data demonstrated the
safety of a more rapid wean through OI comparison, with Improved health-care quality was established by this programme.
feedback by the stewardship team to the clinical team able to This occurred through a decrease in iNO delivery practice varia-
reinforce the safety of the prescribed protocol improving con- tion, reducing unnecessary and potentially harmful exposure
fidence with criteria based weaning. This reinforcement is whilst providing the hospital an economic benefit through safe
believed to have led to the 17% increase in compliance cost reduction strategies.
throughout the second year.
In most instances of protocol non-compliance, notes indi-
Study limitations
cate that the weaning was slowed to ensure patient stability
prior to next wean, or due to imaging unavailability or proto- Data collection for the pre-stewardship programme cohort
col unawareness. Though meeting initiation criteria, nearly occurred through a retrospective collection. Retrospective data col-
10% of neonates were initiated on iNO without CPU of the lection through review of patient files made it difficult to quantitate
heart confirming a PPHN diagnosis; with the initiation classi- variation in practice of iNO weaning from established protocols.
fied as HRF. It was observed that unavailability of point of care Due to the observational nature of the study, correlation
CPU at initiation resulted in patients continuing iNO despite between the revised protocol introduction and reduction of iNO
no clinical response occurring. A delay to commence wean usage cannot be fully attributed with the stewardship pro-
was further observed to await CPU evidence of improvement gramme, rather than an associated trend due to increased proto-
despite patients meeting the weaning criteria in the protocol. col awareness and its usage by staff.
To reduce time to wean further it may be useful to add more The conduct of this study occurred in a single tertiary level NICU,
explicit advice regarding the timing and availability of CPU to with a broad patient demographic across a significant breadth of
the protocol. gestational age and weight, with heterogeneity amongst patient
Changes in the initiation and weaning practices of iNO therapy diagnoses and clinical complexity. This variation provides a short-
within the NICU are likely attributed to increased awareness of term limitation on the interpretation of outcomes, namely referral
the protocol by all staff, the protocol being displayed beside for ECMO and death, in the context of iNO weaning processes.
270 Journal of Paediatrics and Child Health 56 (2020) 265–271

Generalisability and spread 4 Bendapudi P, Rao GG, Greenough A. Diagnosis and management of
persistent pulmonary hypertension of the newborn. Paediatr. Respir.
This study provides evidence that a stewardship programme Rev. 2015; 16: 157–61.
could be safely implemented in any NICU to safely reduce 5 Askie LM, Ballard RA, Cutter GR et al. Inhaled nitric oxide in preterm
iNO usage through protocol compliance, further reinforcing infants: An individual-patient data meta-analysis of randomized trials.
previously published data.9,10 A reduction in iNO therapy Pediatrics 2011; 128: 729–39.
practice variance provides efficiency and cost reduction bene- 6 Cabral JE, Belik J. Persistent pulmonary hypertension of the newborn:
Recent advances in pathophysiology and treatment. J. Pediatr. 2013;
fits to the hospital whilst maintaining safe patient outcomes.
89: 226–42.
Discussions for the implementation of such stewardship
7 Bhatraju P, Crawford J, Hall M, Lang JD. Inhaled nitric oxide: Current
programmes at select Australian NICUs has already
clinical concepts. Nitric Oxide 2015; 50: 114–28.
commenced. 8 Porta NF, Steinhorn RH. Pulmonary vasodilator therapy in the NICU:
Inhaled nitric oxide, sildenafil, and other pulmonary vasodilating
agents. Clin. Perinatol. 2012; 39: 149–64.
Conclusion 9 Elmekkawi A, More K, Shea J et al. Impact of stewardship on inhaled
nitric oxide utilization in a neonatal ICU. Hosp. Pediatr. 2016; 6:
This study concludes that a stewardship programme for iNO use 607–15.
can be implemented in the NICU setting to safely improve proto- 10 Di Genova T, Sperling C, Gionfriddo A et al. A stewardship program to
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reducing economic costs and improving patient safety with no Manag. Health Care 2018; 27: 74–80.
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protocols alongside a stewardship programme promotes nurse- rising costs and high drug expenditures in critical care pharmacy
led care, leads to an overall reduction in total iNO usage and practice. Pharmacotherapy 2017; 37: 54–64.
12 Kinsella JP, Cutter GR, Walsh WF et al. Early inhaled nitric oxide ther-
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doi:10.1111/jpc.

Impact of inhaled nitric oxide stewardship programme in a

What is already known on this topic What this paper adds

Journal of Paediatrics and Child Health 56 (2020) 265–271 265

266 Journal of Paediatrics and Child Health 56 (2020) 265–271

Journal of Paediatrics and Child Health 56 (2020) 265–271 267

Data extraction and analysis

Journal of Paediatrics and Child Health 56 (2020) 265–271 269

Pre-stewardship Post-stewardship P value†

Treatment episodes of iNO given, n 19 21 NA

270 Journal of Paediatrics and Child Health 56 (2020) 265–271

Journal of Paediatrics and Child Health 56 (2020) 265–271 271

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