RESEARCH

1 57
2 58
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4
Nurses Early Recognition of Neonatal 59
60
5
6 Sepsis 61
62
7 63
Michele Boettiger, Lynda Tyer-Viola, and Joseph Hagan Q19
8 64
9 65
10 66
11 Correspondence ABSTRACT 67
Lynda Tyer-Viola, RNC,
12 Objective: To determine nurses perceptions of the most common physiologic and behavioral indicators of neonatal 68
PhD, FAAN, Texas
13 Childrens Hospital, 6651 sepsis. 69
14 Main Street, Suite E, Design: Descriptive correlational study. 70
15 0325.03, Houston,
71
TX 77030. Setting: A womens and childrens hospital in an academic medical center in the southwestern United States.
16 latyervi@texaschildrens.org 72
17 Participants: Nurses (N 181) who cared for neonates in the motherinfant and NICU settings.
73
18 Keywords Methods: Participants completed an e-mail survey developed from the literature to ascertain their perceptions of 74
intuition which physiologic and behavioral indicators were most often associated with neonatal sepsis. Descriptive and infer-
19 75
neonatal
20 ential statistics were used to analyze the data. 76
newborn
21 sepsis Results: Participants identified six signs and symptoms as indicators most often associated with sepsis: two were 77
22 surveillance physiologic and four were behavioral. Recognition of these indicators was not related to level of nursing education but 78
23 was associated with working in the NICU. Seventy-three percent of participants reported that they suspected that 79
24 newborns were septic before evaluation and diagnosis of septicemia. 80
25 Conclusion: Nurses can identify the physiologic and behavioral indicators related to neonatal sepsis. Early recog- 81
26 nition, expressed as their intuitive knowing, should be considered a valuable clinical tool. Understanding that different 82
27 practice settings influence identification of signs and symptoms is important. Integration of this knowledge into formal 83
28 care surveillance could potentially lower the threshold for early evaluation and treatment and thereby improve 84
29 outcomes. 85
30 JOGNN, -, --; 2017. https://doi.org/10.1016/j.jogn.2017.08.007 86
31 Accepted August 2017 87
32 88
33 89
34 90
35 91

N ewborn sepsis remains one of the top 10 (Wynn, 2016). Neonatal sepsis is defined as a
Michele Boettiger, RNC-
36 NIC, MSN, is a patient care 92
37 leading causes of death in neonates in the bacterial infection in the blood classified by day
manager in the NICU, Texas 93
38 Childrens Hospital, United States (Kochanek, Murphy, Xu, & Tejada- of life at diagnosis; early-onset sepsis (EOS) de-
94
39 Houston, TX. Vera, 2016). Seventy-five percent of all neonatal velops in the first 2 to 3 days after birth, and late-
95
40 Lynda Tyer-Viola, RNC, PhD,
deaths worldwide occur during the first week of onset sepsis (LOS) occurs within 3 to 7 days or as
96
41 FAAN, is Assistant Vice life, and 25% to 44% occur within the first 24 hours late as 120 days after birth (Hornik et al., 2012;
97
42
President of Womens Services of life (Voller & Myers, 2016; World Health Wynn, 2016). To prevent harm and improve
and Director of Nursing 98
43 Organization, 2016). Many of these deaths are neonatal outcomes, health care providers should
Research, Texas Childrens 99
44 Hospital Pavilion for Women, attributed to neonatal sepsis, the early and know which newborns and infants are at risk for
100
45 and is an assistant clinical appropriate identification of which could improve sepsis and how to identify those who may be
101
professor, Baylor College of outcomes and avert some neonatal deaths (World decompensating as the result of sepsis as soon
46 Medicine, Houston, TX. 102
47 Health Organization, 2016). Although the inci- as possible. The creation of a care environment in
103
48
Joseph Hagan, ScD, MSPH, dence of sepsis in the United States has which all caregivers have the skills and opportu-
is a statistician in the 104
49 decreased, the consequences of morbidity and nity to intervene early may improve neonatal
Department of Neonatology, 105
50 Texas Childrens Hospital, mortality are great for those who are infected. As outcomes.
106
51 Houston, TX. such, caregivers are required to have a greater
107
level of suspicion and a lower threshold to evaluate
52
newborns and infants for sepsis (Edwards, 2016).
Literature Review 108
53 Q3
Neonates of all gestational ages are vulnerable to 109
54 Diagnosis of sepsis can be difficult because there sepsis because of the immaturity of their immune 110
The authors report no con-
55 ict of interest or relevant are many subtle signs and symptoms, and no systems. When a birth is complicated by maternal 111
56 nancial relationships. consensus exists on defining clinical features comorbid disease or complications of labor or an 112

http://jognn.org 2017 AWHONN, the Association of Womens Health, Obstetric and Neonatal Nurses. 1
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113 169
114 Table 1: Factors Related to Sepsis in the Neonate 170
115 171
Maternal Risk Factors for Infections Clinical Findings Differential Diagnosis
116 172
Group B streptococcus Hyperthermia Herpes simplex virus
117 173
118 Herpes simplex virus Respiratory distress Enteroviruses 174
119 Chorioamnionitis Tachycardia Parechovirus 175
120 Premature rupture of membranes Lethargy Cytomegalovirus 176
121 Prolonged rupture (>18 hours) Poor feeding Influenza viruses 177
122 Multiple gestation Apnea Respiratory syncytial virus 178
123 Gestational infections Poor perfusion Spirochetal infections: 179
124 Vomiting Syphilis 180
125 Jaundice Parasitic infections: 181
126 Hepatomegaly B Congenital malaria
182
127 183
B Toxoplasmosis
128 184
B Fungal infections
129 185
130 186
131 187
132 infant has innate risk factors such as prematurity, vigilance on the part of health care providers in 188
133 the risk for infection increases (Wynn, 2016). their surveillance of newborns at risk. In a pro- 189
134 Because of the lack of specificity of diagnostic spective national study of GBS infection, 81% of 190
135 attributes, the differentiation of sepsis from other mothers of term infants with sepsis had negative 191
136 diagnoses can be problematic and result in a test results for GBS cultures (Stoll et al., 2011). In 192
137 delay of care (Shah & Padbury, 2014). The half of the infants who developed EOS, their GBS- 193
138 maternal risk factors and clinical findings asso- positive mothers had received intrapartum anti- 194
139 ciated with several different diagnoses in neo- biotics (Stoll et al., 2011). 195
140 nates are depicted in Table 1. These overlapping 196
141 signs and symptoms make the early recognition Newborns are also exposed to infection during 197
142 of sepsis difficult. The overall incidence of EOS labor complicated by suspected chorioamnioni- 198
143 and LOS is estimated to be 1 to 2 per 1,000 births tis. All infants of mothers who have fever during 199
144 (Weston et al., 2011). This number is influenced labor are at risk for sepsis, with premature infants 200
145 by gestational age at birth and birth weight. In- having increased risk. Premature infants of 201
146 fections occur more often in preterm infants (4.4 mothers who were treated for chorioamnionitis 202
147 to 6.3 per 1,000 births) than in term infants (.98 were at far greater risk of neonatal infection than 203
148 per 1,000 births; Bailit et al., 2010; Cohen- were premature infants of mothers who were not 204
149 Wolkowiez et al., 2009; Stoll et al., 2011). Very- treated (Ramsey, Lieman, Brumfield, & Carlo, 205
150 low-birth-weight (VLBW) infants (<1,500 g birth 2005). The rate of prematurity in the United 206
151 weight) are at increased risk for sepsis because States decreased from 10.41% to 9.54% of live 207
152 of the immaturity of their immune systems and the births from 2007 to 2014 (Hamilton, Martin, 208
153 interventions necessary for survival that expose Osterman, Curtin, & Matthews, 2015). In 2015 209
154 them to infectious organisms (Hornik et al., 2012). there was a slight increase in preterm births, with 210
155 1 in 10 infants born prematurely (Centers for 211
156 EOS, which can be rapid and fulminating in a Disease Control and Prevention, 2017). Unfortu- 212
157 neonate, is most often attributed to vertical nately, racial and ethnic disparities persist, and 213
158 transmission of contaminated amniotic fluid or the rate of premature birth among Black women is 214
159 bacteria in the mothers urine or genital tract 48% greater than the rate for all other women 215
160 during the intrapartum period (Hornik et al., 2012; (March of Dimes, 2016). Exposure to infection 216
161 Polin, 2012). The incidence of EOS from group B during labor coupled with prematurity may place 217
162 streptococcus (GBS) has been greatly reduced more infants at risk. 218
163 with the change in clinical practice to assess for 219
164 GBS during pregnancy and provide prophylactic LOS is more often attributed to horizontal factors 220
165 antibiotic treatment during labor (Verani, McGee, that occur during prolonged NICU hospitaliza- 221
166 & Schrag, 2010). However, GBS continues to be tions (Stoll et al., 2002). VLBW newborns are 222
167 the leading cause of neonatal sepsis regardless more susceptible to sepsis and have a 223
168 of intrapartum treatment and warrants increased 20% sepsis-related mortality rate (Shane & Stoll, 224

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225 2014; Stoll et al., 2002). Their immature immune 281

226 systems, their underdeveloped central nervous Premature infants who experience prolonged 282
227 systems, and the need for central venous access hospitalization in the NICU are placed at continuous risk 283
228 for treatment make them more vulnerable to for sepsis. 284
229 sepsis (Stoll et al., 2002; Wynn, 2016). The inci- 285
230 dence of LOS is highly dependent on opportunity; 286
231 the longer the period of hospitalization and the function, or appearance. The clinical signs and 287
232 more complicated a newborns health status, the symptoms of neonatal sepsis are often subtle and 288
233 greater the incidence. LOS is associated with nonspecific; thus, they must be distinguished 289
234 other factors that affect sick neonates during their from other conditions (Chapman, 2016; Voller & 290
235 prolonged hospital stays, such as hypoxia, Myers, 2016). Suspicion of sepsis should be 291
236 acidosis, hypothermia, and hypoglycemia (Nizet informed by known risk factors and clinical events 292
237 & Klein, 2010). During these events, neonates that have placed the infant at risk and by labo- 293
238 are vulnerable, and standard-care practices, ratory data (Nizet & Klein, 2010). The early 294
239 such as multiple blood samplings and central line indicators of the development of sepsis are not 295
240 access, create conduits or vectors for infection. well described. If clinicians wait to treat neonates 296
241 Unfortunately, the cycle of care of VLBW neo- who clearly display multiple physiologic signs of 297
242 nates and intensive care events can be ongoing sepsis or changes in behavior, the neonates are 298
243 and can place neonates at continuous risk. placed at greater risk for morbidity and mortality. 299
244 300
245 A definitive diagnosis of sepsis can only be Surveillance for sepsis occurs at the bedside with 301
246 confirmed with positive results from blood the nurse because parents may not recognize the 302
247 cultures (Goldstein, Giroir, & Randolph, 2005). slight changes in the newborn during the imme- 303
248 Recognition of subtle changes early in the infec- diate postpartum period. In the MBU setting, the 304
249 tious process can be challenging because these assessment skills of the motherinfant nurse and 305
250 changes are influenced by the age of the infant, recognition of the subtle changes of sepsis in the 306
251 the infants adjusted gestational age, and the care neonate are the primary tools with which to 307
252 environment. For example, neonates who are recognize developing sepsis. In the NICU, the 308
253 younger than 26 weeks gestation or who weigh diagnosis of sepsis is always lurking but difficult 309
254 less than 2,500 g are often monitored on an open to detect (Rubarth, 2003). In a qualitative study of 310
255 radiant warmer or isolette in the high-surveillance the lived experience of nurses caring for 311
256 setting of a NICU (Hofer, Muller, & Resch, 2012). newborns with sepsis, some participants felt 312
257 This treatment environment often creates fluctu- frustrated when they witnessed the slow deterio- 313
258 ations in the neonates temperature. Neonates in ration of neonates because of sepsis (Rubarth, 314
259 normal newborn settings, such as motherbaby 2003). Other participants believed that they 315
260 units (MBUs), are often wrapped or held skin-to- knew something was wrong but waited for the 316
261 skin by their mothers in private rooms, which neonates to develop more definitive signs and 317
262 may make it difficult for the nurse to observe early symptoms before seeking consultation and need Q4 318
263 changes that indicate illness. Although the likeli- for intervention. Rubarth (2003) concluded that 319
264 hood of sepsis is low in neonates born at term, it experienced nurses seemed to recognize early 320
265 is influenced by and increased in the presence of sepsis through subtle changes in the newborns 321
266 maternal risk factors that include positive test skin color and behavior (p. 35). Deterioration 322
267 results for GBS cultures, herpes simplex virus, may be prevented by recognizing signs and Q5 323
268 and intrapartum factors of maternal temperature symptoms as a cluster versus noting them 324
269 greater than 100.4  F and membranes ruptured separately, which could assist with early 325
270 for more than 18 hours (Puopolo et al., 2011). intervention. 326
271 327
272 Signs and symptoms are important only as they Although several predictive tools and models have 328
273 are viewed in relation to the illness to which they been suggested for early recognition of sepsis, few 329
274 may be attributed (Cox, Ray, Jensen, & Diehl, have been successfully integrated into practice 330
275 2014). A sign is defined in the medical literature (Holme, Bhatt, Koumettou, Griffin, & Winckworth, 331
276 as objective, measureable, and reproducible 2013; Okascharoen, Hui, Cairnie, Morris, & 332
277 (Cox, Ray, Jensen, & Diehl, 2014). A symptom is Kirpalani, 2007; Okascharoen, Sirinavin, 333
278 defined by the International Classification of Thakkinstian, Kitayaporn, & Supapanachart, 334
279 Nursing Practice (2017) as a phenomenon that 2005; Rubarth, 2007). Rubarth (2007) developed 335
280 is a subjective change in the body of sensation, and tested the Newborn Scale of Sepsis. This 336

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337 13-item scale consists of five laboratory tests and requires intervention. The NTS has not been 393
338 eight clinical indicators of sepsis. The instrument externally validated in the literature to date. 394
339 was tested with 62 infants with signs of sepsis or 395
340 risk factors to develop it and had a Cronbach alpha Understanding which physiologic and behavioral 396
341 coefficient of 0.65. The results indicated high indicators nurses perceive to be most often 397
342 sensitivity (93%) yet low specificity (47%) and low indicative of sepsis is a first step to improve care. 398
343 positive predictive value (29%), which showed it to The purpose of our study was to identify the 399
344 be limited in its usefulness as a diagnostic tool. physiologic and behavioral indicators that nurses 400
345 Okascharoen et al. (2005) developed the bedside believe are most often the signs and symptoms of 401
346 prediction scoring model for late-onset neonatal neonatal sepsis from the common indicators 402
347 Q6 sepsis through the use of derivation analysis with noted in the literature. Our research questions 403
348 1,870 neonates who stayed in the hospital more were as follows: What are the most common 404
349 than 72 hours. Using regression modeling, seven physiologic and behavioral indicators that nurses 405
350 variables were found to explain late-onset neonatal identify with neonatal sepsis? How frequently did 406
351 sepsis when it occurred: hypotension, abnormal a nurse think that a neonate was septic who was 407
352 body temperature, respiratory insufficiency, later diagnosed with sepsis? Is there a relation- 408
353 neutrophil bandemia, thrombocytopenia, a dose ship between the characteristics of a nurse (level 409
354 measure of the presence of an umbilical venous of nursing education, years of nursing experi- 410
355 Q7 catheter of fewer than or more than 7 days, and ence, or current practice setting) and the in- 411
356 lethargy. The measure of lethargy, although pre- dicators that the nurse most often identified as 412
357 sent in all cases, was removed because it was being related to neonatal sepsis? 413
358 subjectively measured. When removed, it did not 414
359 change the models accuracy. These researchers 415
360 tested the model with a validation sample and
Methods 416
361 found no differences in its sensitivity and speci- Study Design and Setting 417
362 ficity to predict late-onset neonatal sepsis before We conducted a descriptive correlational study in 418
363 positive results of blood cultures in risk groups a large academic womens and childrens hospital 419
364 (Okascharoen et al., 2007). Use of this tool showed in the southern United States. The setting 420
365 high negative predictive value (90% to 96%) but included a 173-bed NICU equipped to provide Q8 421
366 low positive predictive value (56% to 43%). This Level II to Level IV surgical care for infants born at 422
367 tool shows promise for the identification of children the hospital or transferred to the hospital from 423
368 who do not have sepsis, yet it is highly dependent throughout the United States. All infants in the 424
369 on physiologic data variation that may occur later NICU, regardless of whether they are on radiant 425
370 in the trajectory of sepsis than the subtle behavioral warmers or in isolettes or bassinets, are centrally 426
371 changes that can be observed earlier. monitored. Clinicians in the 5-year-old obstetric 427
372 service provide all levels of obstetric care, with 428
373 Although not specific to sepsis, Holme and col- 6,000 births annually in a patient-centered care 429
374 leagues (2013) evaluated a tool to identify unwell model. The admission rate of infants born at the 430
375 neonates. The Neonatal Trigger Score (NTS) was hospital to the NICU is 21%. The MBU consists of 431
376 evaluated in 485 neonates older than 35 weeks 48 private rooms and 2 respite nurseries. The 432
377 gestation who were admitted to the NICU and nurses provide couplet care with newborns at 433
378 matched with age-appropriate well newborns. their mothers bedsides. The respite nurseries are 434
379 The NTS was used to evaluate compulsory mea- used for infants who require closer observation or 435
380 sures of temperature, pulse, respiratory rate, when families request their infants go to the 436
381 respiratory distress, level of consciousness, and nursery. As a Baby-Friendly hospital, the goal is 437
382 blood glucose level before feeding. Level of to practice rooming-in, which allows mothers and 438
383 consciousness is an objective measure because infants to remain together unless a greater level of 439
384 it includes choosing a description of being active, care is clinically necessary (Ward, Williamson, 440
385 floppy, flaccid, lethargic, or irritable. This scoring Burke, Crawford-Hemphill, & Thompson, 2017). 441
386 system holds promise because it is focused on This model supports the tenets of early bonding 442
387 the neonate, with 77% sensitivity and 97% speci- with skin-to-skin care and exclusive 443
388 ficity of identifying newborns who require evalu- breastfeeding. 444
389 ation and admission to the NICU. In addition, the 445
390 tool identified 19 well newborns for evaluation. Of Survey Development 446
391 those, 13 had triggers of low temperature, which The study survey was developed through the use 447
392 is a common condition in the first 12 hours but of content and face validity methods by 448

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449 incorporating a review of the literature and prac- included indicators that are objective and quanti- 505
450 tice expertise. Clinical findings related to neonatal fied by standardized measurements or machines. 506
451 sepsis found in the literature are listed in Table 2 Behavioral items included subjective indicators 507
452 (Nizet & Klein, 2010; Stoll et al., 2011). A sample that are evaluated and described according to the 508
453 survey of 27 items was created from these known degree of their presence. For example, jaundice is 509
454 clinical findings on the basis of the language and described by color and intensity. If it were quan- 510
455 descriptions commonly used by bedside nurses. tified, it would be measured as a bilirubin level. 511
456 For example, poor response to painful stimuli in a The survey was distributed to six experts in 512
457 term infant would be viewed as lethargy. The neonatal care for evaluation of content and face 513
458 items were phrased as questions, How often to validity. After careful review of the experts feed- 514
459 you consider [blank] as an indicator of sepsis? or back, we removed two questions. The final survey 515
460 as statements to elicit a level of agreement, consisted of 25 questions related to how often a Q10 516
461 Decreased muscle tone is an indicator of nurse considered a behavioral or physiologic 517
462 newborn sepsis. Responses to items were characteristic to be an indicator of sepsis (see 518
463 categorized as never, not often, often, or very Appendix S1, provided as supplemental material 519
464 often for some items and never, sometimes, to the online version of this article). 520
465 frequently, or always for other items. Choices 521
466 were recorded as numeric scores of 1 to 4, and a Participants 522
467 greater score indicated that the characteristic Approval for research with human participants Q11 523
468 was believed to be more frequently an indicator of was granted by the Baylor College of Medicine 524
469 newborn sepsis. Items were categorized as Internal Review Board before participant enroll- 525
470 physiologic (8 items) or behavioral (18 items) in- ment. Registered nurses who worked in the NICU 526
471 Q9 dicators. Items had slight differences, with the or the MBU were eligible to participate. Nurses 527
472 intention to use language that is used in different were excluded if they functioned as advanced 528
473 care settings by different nurses. For example, practice nurses. Use of an a priori power analysis 529
474 flaccidity versus decreased muscle tone: the indicated that the anticipated response rate of 530
475 former is used more commonly by NICU nurses 40% from the 475 potential participants to whom 531
476 and the latter by MBU nurses. Physiologic items the survey was distributed would yield 190 532
477 completed surveys. The expected 190 survey 533
478 responses would provide 80% statistical power to 534
479 detect, at the 5% significance level, a true cor- 535
480 Table 2: Clinical Findings Associated With relation of r .202. This represents a small-to- 536
481 Neonatal Sepsis medium effect size according to Cohens (1988) 537
482 conventional criteria. 538
Finding
483 539
484 Hyperthermia Procedures 540
485 Respiratory distress The survey was prepared in SurveyMonkey for 541
486 e-mail distribution with a cover letter in which 542
Tachycardia
487 anonymous participation was requested. The re- 543
Lethargy
488 searchers posted signs in the NICU and MBU to 544
489 Poor feeding encourage nurses to participate. The survey 545
490 Bradycardia included the following instructions: The following 546
491 are questions related to your nursing practice. 547
Poor perfusion/hypotension
492 Please read the questions and responses care- 548
493 Vomiting fully and select the response you use in your 549
494 Jaundice nursing care. The nurses in the NICU care for 550
495 term and preterm newborns. The nurses in the 551
Hepatomegaly
496 MBU care for newborns older than 36 weeks 552
497 Cyanosis gestation. After 2 weeks, the survey link was 553
498 Hypothermia e-mailed again to encourage additional re- 554
499 sponses. The average time for the nurses to 555
Irritability
500 complete the survey was less than 5 minutes. 556
501 Seizures 557
502 Abdominal distention Analysis 558
503 Diarrhea Participant characteristics and survey items were 559
504 examined with the use of descriptive statistics 560

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561 and the Kruskall-Wallis test to determine differ- 617

562 ences between characteristics. Items with mean Table 3: Characteristics of Participants 618
563 scores greater than 3.0, which signified that (N [ 181) Q1
619
564 indicators were present often or very often or 620
Characteristics n (%)
565 frequently or always, were the most recognized 621
Sex
566 indicators of sepsis. Spearmans correlation was 622
567 used to assess the associations among highest Female 179 (99) 623
568 education level in nursing, years of nursing Male 2 (1) 624
569 experience, and frequency with which the most 625
Age (years)
570 recognized physiologic and behavioral indicators 626
571 were identified with neonatal sepsis. The <30 46 (28) 627
572 Wilcoxon rank sum test was used to determine 3039 59 (36) 628
573 whether the frequency with which the most often 629
4049 36 (22)
574 recognized indicators of neonatal sepsis differed 630
575 by practice area (MBU versus NICU). Statistical 5059 16 (10) 631
576 Analysis System (SAS) version 9.4 was used for $60 7 (4) 632
577 all data analysis. 633
Years practicing as a nurse
578 634
579 Results <10 74 (43) 635
580 The survey was distributed to 475 registered 1019 51 (29) 636
581 nurses. The response rate was 38% (N 181). 2029 39 (22)
637
582 Most participants were female (99%), their 638
$30 10 (6)
583 average age was 37.3 years, and, on average, 639
584 they had 13.2 years of experience in nursing (see Ethnicity 640
585 Table 3). Limited differences related to specific White 103 (59) 641
586 characteristics overall were found. Hispanic/ 642
Black 20 (11)
587 Latino participants believed that irritability, such 643
588 as arching of the back in a term infant, was less Asian 36 (20) 644
589 frequently an indicator of newborn sepsis than Hispanic/Latino 10 (6) 645
590 did participants of other ethnicities (c2 13.0, 646
Other 7 (4)
591 df 5, p .022). Black participants and those 647
592 who indicated other as their ethnicities consid- Highest education level in nursing 648
593 ered newborn seizure to be an indicator of sepsis Diploma 3 (2) 649
594 more frequently than did those of other ethnic 650
Associate Degree in Nursing 34 (19)
595 groups (c2 12.0, df 5, p .035). 651
Bachelor of Science in Nursing 128 (72)
596 652
597 The items in the survey were all indicators of Master of Science in Nursing 14 (8) 653
598 sepsis. Participants were asked to indicate which Current area of practice 654
599 items were more often or most frequently 655
MotherBaby Unit 30 (17)
600 Q12 indicators of sepsis. Our participants chose six 656
601 indicators of sepsis that were perceived to be NICU 151 (83) 657
602 present more than frequently or often (items with 658
603 mean scores $3): lethargy and poor response to 659
604 painful stimuli by a term infant (a form of leth- 660
605 argy), increased occurrence of apnea, irritability responded that they very often (n 82) or often Q13 661
606 such as increased labor of breathing, increased (n 25) thought a newborn was septic before the 662
607 flaccidity, and temperature of at least 100.2  F newborn was examined and diagnosed with 663
608 that lasts more than 2 hours. The descriptive sepsis; 27% of participants responded that they 664
609 statistics for responses to items that correspond had this experience not often (n 38) or never 665
610 to physiologic data and behavioral characteris- (n 3). Participants from the NICU reported 666
611 tics of neonatal sepsis are displayed in Table 4. caring for newborns who they thought were sep- 667
612 tic and who were later diagnosed with sepsis 668
613 Participants were asked How often have significantly more often than did participants from 669
614 you cared for a child who you thought was the MBU (p < .001). We found no relationships 670
615 septic, who was later diagnosed with sepsis? between the level of nursing education and the 671
616 Seventy-three percent of participants (107/148) six indicators that were chosen as more often or Q14 672

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673 729
674 Table 4: Descriptive Statistics of Participant Responses to Physiologic and Behavioral 730
675 Characteristics of Neonatal Sepsis 731
676 732
Survey Item (Category) M SD
677 733
Lethargy (B) 3.4 0.6
678 734
679 Poor response to painful stimuli by a term infant (B) 3.1 0.8 735
680 Increased occurrences of apnea (P) 3.0 0.7 736
681 737
Irritability such as increased labor of breathing (B) 3.0 0.7
682 738
683 Increased flaccidity (B) 3.0 0.8 739
684 Temperature $100.2  F lasting >2 hours (P) 3.0 0.7 740
685 741
Noniatrogenic (not caused by medication) temperature (P) 2.9 0.7
686 742
687 Respiratory distress (B) 2.9 0.7 743
688 Poor capillary refill (P) 2.8 0.8 744
689 745
Abdominal distention (B) 2.8 0.7
690 746
691 Mottling (B) 2.7 0.7 747
692 Tachycardia lasting more than 4 hours (P) 2.7 0.7 748
693 Hypoglycemia (P) 2.7 0.7
749
694 750
Decreased muscle tone (B) 2.7 0.7
695 751
696 Increased signs of irritability (B) 2.6 0.7 752
697 Tachypnea lasting more than 2 hours (P) 2.6 0.7 753
698 754
Respiratory distress such as grunting or retractions (B) 2.6 0.7
699 755
700 Alteration in blood pressure (P) 2.5 0.7 756
701 Seizure (B) 2.4 0.7 757
702 758
Feeding intolerance such as emesis after feedings (B) 2.3 0.6
703 759
704 Loose stool (B) 2.3 0.6 760
705 Poor suck and swallow during feeding (B) 2.1 0.6 761
706 762
For a term infant, irritability such as arching of the back (B) 2.1 0.7
707 763
Inconsolable crying (B) 2.0 0.6
708 764
709 Bruising (B) 1.9 0.7 765
710 Jaundice (B) 1.7 0.5 766
711 767
712 Note. A higher mean indicates the characteristic is believed to be more frequently an indicator of newborn sepsis on a scale of 768
1 never; 2 sometimes/not often; 3 frequently/often; and 4 always/very often. B behavioral; M mean; P physiologic;
713 SD standard deviation. 769
714 770
715 771
716 772
717 773
718 always indicative of physiologic and behavioral more often than did nurses in the MBU (see 774
719 indicators of sepsis. There was a weak relation- Table 5). 775
720 ship between years of experience and recogni- 776
721 tion of lethargy as an indicator of sepsis (r .273, 777
722 p < .001). We found significant differences be- Discussion 778
723 tween the current practice setting and the top six We examined nurses perceptions of the most 779
724 indicators that were chosen as often or very often commonly recognized physiologic and behav- 780
725 or frequently or always indicative of sepsis by ioral indicators of sepsis. Early recognition of the 781
726 participants. Participants in the NICU considered subtle and less specific signs and symptoms of 782
727 response to painful stimuli, apnea, and increased neonatal sepsis may improve treatment and 783
728 flaccidity in term infants as indicators of sepsis long-term outcomes. Behaviors identified by 784

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785 841
786 Table 5: Differences Between Recognized Sepsis Indicators and Practice Area 842
787 843
Practice Area
788 844
789 MotherInfant Unit 845
790 (n 30) NICU (n 151) 846
791 847
792 Q2 Sepsis Indicator M SD M SD p 848
793 How often do you consider lethargy as an 3.2 0.8 3.5 0.6 .244 849
794 indicator of newborn sepsis? 850
795 851
How often do you consider poor response 2.5 0.8 3.3 0.7 <.001*
796 852
to painful stimuli by a term infant an
797 853
indicator of sepsis?
798 854
799 Increased occurrence of apnea by the 2.7 0.8 3.1 0.6 .005* 855
800 newborn is considered an indicator of 856
801 neonatal sepsis. 857
802 Irritability such as increased labor of 2.9 0.9 3.0 0.6 .463 858
803 breathing indicates newborn sepsis.
859
804 860
How often do you consider increased 2.7 0.9 3.0 0.8 .040*
805 861
flaccidity as an indicator of sepsis?
806 862
807 A newborn temperature of 100.2  F or 3.0 0.9 3.0 0.7 .662 863
808 greater lasting for longer than 2 hours is 864
809 considered an indicator of sepsis. 865
810 866
Note. M mean; SD standard deviation.
811 *p < .05. 867
812 868
813 869
814 870
815 participants included lethargy, irritability, and Morgan & Wright, 2007; Solevag, Eggen, 871
816 flaccidity, which may appear before the common Schroder, & Nakstad, 2013). Morgan et al. 872
817 findings of hyperthermia, respiratory distress, (1997) described an early-warning system 873
818 and tachycardia (Nizet & Klein, 2010; Stoll et al., (EWS) to detect the development of critical illness 874
819 2011). Differences in practice settings should that has been modified for use in many 875
820 be considered when defining nursing care such populations. The EWS was designed solely to 876
821 as nursing assessment and triggers for reporting secure the timely responses of clinicians to their 877
822 slight deviations. Participants reported that their patients bedsides. For pediatric patients, these 878
823 suspicions of sepsis were often correct. It may be systems are best used to detect decompensation 879
824 Q15 important to use the most commonly recognized with respiratory and cardiovascular collapse 880
825 signs and symptoms identified by nurses to (Solevag et al., 2013). The use of a system to 881
826 standardize sepsis surveillance. When the ability identify neonatal sepsis that is based solely on 882
827 to identify infants at risk for sepsis is potentially physiologic changes is challenging because 883
828 affected by the experience of a nurse and the several differential diagnoses could be present in 884
829 practice setting, the use of clinical tools and a newborns first week of life (Chapman, 2016). 885
830 routine surveillance standards to improve care is 886
831 important. Participants in our study identified three of the 887
832 triggers used to develop the early-recognition 888
833 Deterioration of patients is often preceded by NTS: temperature, respiration (increased occur- 889
834 physiologic changes or changes identified by rence of apnea), and level of consciousness 890
835 family or nurses (Chapman, 2016; Subbe, Kruger, (lethargy/flaccidity; Holme et al., 2013). The indi- 891
836 Rutherford, & Gemmel, 2001), and implementa- cator irritability, such as increased labor of 892
837 tion of physiologic surveillance frameworks for breathing, could have also been perceived as a 893
838 evaluation and treatment of adults and children change in respiratory rate. Of interest, our find- 894
839 who may be at risk for decompensation are well ings and the NTS include change in behavior as a 895
840 described (Morgan, Williams, & Wright, 1997; valid indicator. In an infant, decompensation is 896

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 Boettiger, M., Tyer-Viola, L., and Hagan, J. RESEARCH

897 often first signaled by a change in behavior 953

898 (Odell, Victor, & Oliver, 2009). Good clinical Nurse recognition of indicators of neonatal sepsis was 954
899 practice requires the integration of the subjective influenced by practice area. 955
900 status of the infant into the overall clinical sce- 956
901 nario of the infant. We propose that these cues 957
valid measure in the assessment of infants for
902 often appear earlier, and, when present with risk 958
sepsis, there is the potential to positively influ-
903 factors, the cues should be treated with the same 959
ence outcomes related to this safety issue.
904 weight and concern as physiologic changes. 960
905 961
Nurse intuition is often stated as nurses worry
906 Participants in our study stated that they often 962
and concerns (Douw, et al., 2015). These con-
907 thought a child was septic before the child was 963
cerns are formed from recognition of signs and
908 diagnosed. Nurses may often believe that 964
symptoms and informed by experience, and they
909 something is not right with a patient, and this 965
result in a nurse knowing there is something
910 perception may be present before changes are 966
wrong. Participants in this study who practiced in
911 seen in the physiologic indicators used as the 967
the NICU had extensive experience. Their suspi-
912 triggers for evaluation of deterioration (Douw 968
cions of sepsis may have been based on their
913 et al., 2015). Among our participants, more 969
experiences over time. Douw and colleagues
914 NICU nurses than MBU nurses reported this 970
(2015) conducted a systematic review of signs
915 experience, which is not surprising because 971
and symptoms that reflected concern and worry.
916 newborns in the NICU are at greater risk for 972
They determined that worry and concern can be
917 sepsis. Nurses may have these feelings when 973
present with or without vital sign changes, which
918 they conduct surveillance, which is different from 974
supports the concept of intuitive knowing as a
919 monitoring. Surveillance is the purposeful and 975
trigger to evaluate a patient. NICU nurses may
920 ongoing acquisition, interpretation, and synthesis 976
have developed intuitive knowing related to their
921 of patient data for clinical decision making 977
experiences in caring for more newborns with
922 (Dochterman & Bulechk, 2004). In different care 978
sepsis. Trauma nurses have shown this specialty- Q16
923 settings, nurses implement surveillance that is 979
specific intuition to be valuable and have inte-
924 based on individual perceptions, patient-specific 980
grated it into their initial patient assessments,
925 frameworks of care, and the cognitive process of 981
which resulted in improvements to the correct
926 integrating information (Kelly & Vincent, 2011). 982
identification of injury severity in trauma patients
927 Four themes were identified related to nurse sur- 983
(Cork, 2014). Integration of the feeling that a
928 veillance: Recognition, Recording and Review- 984
newborn may be developing sepsis into an
929 ing, Reporting, and Acting (Odell et al., 2009). 985
acceptable and respected trigger alert system
930 Odell et al. (2009) also noted that within this 986
may enhance early recognition.
931 framework, recognition of deterioration of a pa- 987
932 tient included intuition or observations that were 988
Couplet care for well newborns promotes and
933 incongruent with the patients identified needs. 989
health and well-being of families. Newborns
934 Intuition, as applied to nursing practice, is a well- 990
should be with their mothers throughout the
935 known attribute of Benners framework of Novice 991
postpartum experience to promote exclusive
936 to Expert (Benner, 2001; Green, 2012). Nurses 992
breastfeeding and family bonding. Nursing
937 who are proficient experts integrate intuition into 993
assessment of newborns, in particular those
938 their work on the basis of years of experience in 994
whose mothers have been treated for suspicion of
939 clinical decision making. 995
chorioamnionitis in labor or who develop a fever
940 996
immediately postpartum, should include
941 Nurse intuition should be viewed as a valid form 997
increased surveillance.
942 of knowledge (Green, 2012). Nurses often try to 998
943 validate intuitive knowing with each other rather 999
944 than reporting to the medical care team. Benner Limitations 1000
945 (1984) suggested that nurses were worried Our study had several limitations that restrict its 1001
946 about gaining credibility with physicians, and generalizability; specifically, our participants 1002
947 correct early warning would increase the likeli- were from one large hospital. The findings are 1003
948 hood that physicians would take their vague informed by a care system with a delivery volume 1004
949 concerns more seriously in the future. Concerns of 6,000 births annually and a 173-bed NICU. The 1005
950 about credibility may continue to limit the ways recruitment strategy included self-selection for 1006
951 nurses communicate their concerns about participation. Nurses who were more interested in 1007
952 patients. However, if intuition is incorporated as a the topic overall may have participated, thereby 1008

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1009 should include a retrospective analysis of infants 1065

1010 Physiologic and behavioral indicators and a nurses diagnosed with sepsis to assess how these 1066
1011 intuition that something is wrong can be used to develop a indicators may have been present in newborns 1067
1012 neonatal early warning system for sepsis. before diagnosis and treatment. This analysis 1068
1013 should include any indication that a nurse was 1069
1014 worried or concerned. Creating tools to improve 1070
skewing the results to include those nurses who
1015 surveillance is important to close the identified 1071
care for newborns with sepsis more often. There
1016 practice gap related to model of care delivery 1072
were more NICU than MBU nurse participants,
1017 and years of experience. 1073
which created a bias of nurses who have cared
1018 1074
for more newborns with sepsis. We did not reach
1019 1075
our a priori enrollment target of 190 participants. Conclusion
1020 1076
Last, there was a limitation related to the survey Advances in perinatal care have resulted in a
1021 1077
that we developed for our study. Items were tremendous decrease in the rate of neonatal
1022 1078
phrased to elicit unique understanding not sepsis; however, it continues to be a concern
1023 1079
related to term or preterm infants. For example, because of the associated high rates of morbidity
1024 1080
flaccidity is an expected finding in a premature and mortality. Our findings suggest that the most
1025 1081
infant and also a sign of sepsis. common physiologic and behavioral indicators of
1026 1082
neonatal sepsis recognized by nurses, coupled
1027 1083
with an indicator of concern, could be used to
1028 Implications 1084
develop a new EWS for neonatal sepsis. If these
1029 With the standardization of treatment of GBS- 1085
observations are incorporated into a best-
1030 positive mothers in labor, the suspicion for 1086
practice alert used in electronic medical
1031 sepsis in newborns has been lowered, although 1087
records, clinicians may be able to identify new-
1032 GBS continues to be a cause of sepsis (Stoll 1088
borns who are septic earlier and intervene to
1033 Q17 et al., 2011). When assessing a newborn, 1089
improve outcomes. Specifically, the incorporation
1034 ensuring that NICU nurses are aware of the 1090
of behavioral changes as key indicators and the
1035 mothers GBS status and that they consider it 1091
engagement of parents in observing for these
1036 regardless of whether she has been treated is 1092
changes may create a better warning system.
1037 crucial. The time intervals between full assess- 1093
Nurses are well positioned at the bedside to
1038 ments of newborns should possibly be increased 1094
recognize these behavioral cues early through
1039 for those whose mothers were treated for GBS 1095
the use of their knowledge and intuition. They are
1040 because incidents of EOS from GBS still occur in 1096
also the key caregivers to engage parents.
1041 term newborns. To avert potential delayed 1097
Formal engagement of parents in recognizing
1042 diagnosis of sepsis in a newborn in the MBU, it is 1098
changes in their newborns will improve care of all
1043 imperative to consider the creation of a contin- 1099
newborns. Q18
1044 uous evaluation tool based on the mothers risk 1100
1045 factors including GBS, regardless of treatment. 1101
1046 This tool could also be used to engage new Supplementary Material 1102
1047 parents in observing for subtle changes in all Note: To access the supplementary material that 1103
1048 settings. Use of a neonatal EWS tool that includes accompanies this article, visit the online version 1104
1049 these indicators would bring clinicians to the of the Journal of Obstetric, Gynecologic, & 1105
1050 bedside earlier to assess the need for Neonatal Nursing at http://jognn.org and at 1106
1051 intervention. https://doi.org/10.1016/j.jogn.2017.08.007. 1107
1052 1108
1053 With the wide adoption of electronic medical 1109
1054
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