PLoS ONE plos plosone PLOS ONE 1932-6203 Public Library of Science San Francisco, CA USA 10.1371/journal.pone.0285828 PONE-D-22-21860 Research Article Medicine and health sciencesClinical medicineSigns and symptomsAsphyxia Biology and life sciencesDevelopmental biologyNeonates Medicine and health sciencesWomen's healthMaternal healthBirthLabor and delivery Medicine and health sciencesWomen's healthObstetrics and gynecologyBirthLabor and delivery Medicine and health sciencesHealth careHealth care providers Medicine and health sciencesWomen's healthMaternal healthBirth Medicine and health sciencesWomen's healthObstetrics and gynecologyBirth Medicine and health sciencesCritical care and emergency medicineResuscitation Computer and information sciencesData managementData visualizationInfographicsCharts Medicine and health sciencesWomen's healthMaternal healthNeonatal care Medicine and health sciencesPediatricsNeonatologyNeonatal care Medicine and health sciencesHealth careNeonatal care A comparative analysis of APGAR score and the gold standard in the diagnosis of birth asphyxia at a tertiary health facility in Kenya APGAR score effectiveness in diagnosis of birth asphyxia https://orcid.org/0000-0002-6407-7379 Njie Albertine Enjema Conceptualization Data curation Formal analysis Investigation Methodology Project administration Validation Writing – original draft 1 * Nyandiko Winstone Mokaya Conceptualization Formal analysis Investigation Methodology Supervision Writing – original draft Writing – review & editing 1 2 Ahoya Phinehas Ademi Conceptualization Data curation Formal analysis Investigation Supervision Writing – original draft Writing – review & editing 3 Moutchia Jude Suh Conceptualization Data curation Methodology Validation Visualization Writing – original draft Writing – review & editing 4 Department of Child Health and Pediatrics, College of Health Sciences—Moi University, Eldoret, Kenya Academic Model Providing Access to Healthcare, Eldoret, Kenya Directorate of Child Health and Pediatrics, Moi Teaching and Referral Hospital, Eldoret, Kenya Department of Biostatistics, Epidemiology and Informatics -Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pennsylvania, United States of America Olorunfemi Gbenga Editor University of the Witwatersrand Johannesburg Faculty of Health Sciences, SOUTH AFRICA

The authors have declared that no competing interests exist.

 * E-mail: njieenjema@gmail.com 24 5 2023 2023 18 5 e0285828 4 8 2022 3 5 2023 2023 Njie et al This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Background

Birth asphyxia is a consistent key contributor to neonatal morbidity and mortality, notably in sub-Saharan Africa. The APGAR score, though a globally used diagnostic tool for birth asphyxia, remains largely understudied especially in resource-poor settings.

 Objective

This study determined how effectively the APGAR score is used to diagnose birth asphyxia in comparison to the gold standard (umbilical cord blood pH <7 with neurologic involvement) at Moi Teaching and Referral Hospital (MTRH), and identified healthcare provider factors that affect ineffective use of the score.

 Methods

Using a quantitative cross-sectional hospital-based design, term babies born in MTRH who weighed ≥2500g were randomly and systematically sampled; and healthcare providers who assign APGAR scores were enrolled via a census. Umbilical cord blood was drawn at birth and at 5minutes for pH analysis. APGAR scores assigned by healthcare providers were recorded. Effective use of the APGAR score was determined by sensitivity, specificity, positive and negative predictive values. At a significance level of 0.05, multiple logistic regression analysis identified the independent provider-associated factors affecting ineffective use of the APGAR score.

 Results

We enrolled 102 babies, and 50 (49%) were females. Among the 64 healthcare providers recruited, 40 (63%) were female and the median age was 34.5years [IQR: 31.0, 37.0]. Assigned APGAR scores had a sensitivity of 71% and specificity of 89%, with positive and negative predictive values of 62% and 92% respectively. Healthcare provider factors associated with ineffective APGAR score use included: instrumental delivery (OR: 8.83 [95% CI: 0.79, 199]), lack of access to APGAR scoring charts (OR: 56.0 [95% CI: 12.9, 322.3]), and neonatal resuscitation (OR: 23.83 [95% CI: 6.72, 101.99]).

 Conclusion

Assigned APGAR scores had low sensitivity and positive predictive values. Healthcare provider factors independently associated with ineffective APGAR scoring include; instrumental delivery, lack of access to APGAR scoring charts, and neonatal resuscitation.

 The author(s) received no specific funding for this work. Data Availability All relevant data are within the paper and its Supporting Information files. Introduction

Perinatal mortality is still a significant public health issue, with its top three aetiologies identified as; prematurity (28%), neonatal infections (26%), and birth asphyxia (23%) [1,2]. Birth asphyxia is a neonatal condition characterized by failure to initiate or sustain breathing at birth, and it has been a consistent major aetiology of neonatal deaths in the last decade [3]. Globally, neonatal mortality accounts for about half of under-five mortality [4]. From 2003–2014, childhood mortality trends in Kenya showed that, among neonatal, infant, and under-5 mortalities, neonatal deaths showed the slowest decrease [5]). Therefore, to decrease the mortality rate of children below five years of age, it is imperative to decrease these neonatal deaths [6]. To further curb neonatal mortality, there is a profound need to explore its key aetiologies such as birth asphyxia, especially in resource-poor settings [7]. Sub-Saharan countries bear the greatest burden of birth asphyxia, and these asphyxia-related deaths are for the most part preventable [8].

The APGAR score, though widely used for birth asphyxia diagnosis can either overestimate or underestimate asphyxia due to its subjective nature [9]. The combined APGAR score has shown some superiority to the conventional APGAR score in birth asphyxia diagnosis [10,11], and over the years, severely asphyxiated babies have been found to have normal conventional APGAR scores [9,12]. However, in low- and middle- income countries, the conventional APGAR score continues to be solely used for birth asphyxia diagnosis. An APGAR score of <7 depicts asphyxia; to ascribe this asphyxia to an intrapartum hypoxic-ischemic event, the American College of Obstetricians and Gynecologists and American Academy of Pediatrics require an add-on umbilical cord pH value of <7, evidence of neurologic involvement (e.g., seizures, altered tone, coma) and evidence of multiorgan involvement [13]. Umbilical cord blood pH has also been shown to have better diagnostic value in birth asphyxia [14,15], and when combined with the APGAR score, higher sensitivity in birth asphyxia diagnosis has been observed [16,17].

Birth asphyxia is a major contributor to neonatal morbidity and mortality. Globally, it contributes to a quarter of all neonatal deaths. In Kenya, according to the KDHS 2014 report, birth asphyxia is the leading cause of neonatal deaths at 31.6% [5]. Its consistent unfavorable effect on neonatal mortality in the last decade [18], highlights the need to assess the performance of APGAR score as a diagnostic tool for birth asphyxia in comparison to the gold standard. Failure to optimally diagnose birth asphyxia directly interferes with the timeline of managing these neonates, thereby increasing the risk of neonatal mortality and development of asphyxia-related morbidity.

Published studies report varying proportions of APGAR score sensitivities and specificities of 62.8–99% and 41–81% respectively [11,19,20]. Consistency in APGAR scoring among healthcare providers has been shown to also vary greatly, with the heart rate component of the score having the least inconsistency. Healthcare provider factors influencing APGAR scoring include among others: years of experience of the healthcare provider, cadre of the healthcare provider, number of staff per delivery, nature of resuscitation done by healthcare provider, and the type of delivery [21–23]. Exploring these factors in this study is pivotal in fostering improved usage of the APGAR score by healthcare providers in identifying neonates with asphyxia.

Improvements in antenatal care, delivery and neonatal resuscitation services have been observed in many countries with developing economies. This has led to the establishment of national intervention programs such as “Help Babies Breathe” in Kenya [24,25]. Yet, birth asphyxia consistently remains a major cause of neonatal mortality, creating the need for effective use of its diagnostic tools such as the APGAR score. If the diagnosis of birth asphyxia is not effectively done, it cannot be promptly and adequately managed. Consequently, its short- and long-term morbidity, and mortality persistently occur as reflected by the above-mentioned data. This study therefore aimed to determine how effectively the APGAR score is applied in the labour ward and theatre of a tertiary hospital in Kenya. Furthermore, it assessed healthcare provider factors associated with this effective use of APGAR score. This knowledge will aid in addressing and halting asphyxia-related morbidity and mortality through evidence-based data.

 Materials and methods

This was an analytical cross-sectional hospital-based quantitative study carried out in the labour ward, delivery rooms and theatre of Moi Teaching and Referral Hospital (MTRH), Eldoret, between June 2021 and October 2021. The hospital is a level 6 public hospital and is currently the second largest national teaching and referral hospital in Kenya. Its delivery unit, obstetrics theatre and newborn unit (NBU) are located at the Riley Mother and Baby wing of the hospital. An average of 750 deliveries are carried out and approximately 250 babies are admitted to NBU monthly, creating an optimal study setting for birth asphyxia.

The Karimollah formula for accuracy studies [26] was used to estimate the sample size for this study, using a pre-study estimate of 81% sensitivity and specificity obtained by Dalili and collaborates in their study [11]. The sampling interval (k) calculated for this study was 2. Therefore, the researchers randomly and systematically sampled 102 term neonates (37-42weeks gestation) who had a birthweight of at least 2500 grams. Neonates with life-threatening malformations were excluded because the APGAR score has been shown to be influenced by congenital malformations [15,27]; while, neonates at risk of anaemia/sepsis in the immediate postnatal period were excluded as these could alter umbilical cord blood pH values [28]. Details on neonatal recruitment are demonstrated on Fig 1 below.

10.1371/journal.pone.0285828.g001 Neonatal inclusion flow chart.

To assess healthcare provider factors, 64 healthcare providers who assign APGAR scores to neonates after delivery were enrolled via a census, due to the definite number of healthcare providers in the unit. Interviewer-administered semi-structured questionnaires (S1 File) were used to collect neonatal sociodemographic and clinical characteristics. To collect information on healthcare provider sociodemographic and factors influencing APGAR scoring among healthcare workers, a self-administered questionnaire (S2 File) was used. Umbilical cord blood was collected at birth and in the fifth minute of life from the neonates for pH analysis. This was in accordance to the Standard operating procedure (SOP) adapted from the 2015 guidelines of the Research Centre for Women’s and Infants’ Health (RCWIH) BioBank in Canada for umbilical cord blood collection (S3 File). APGAR scores in the first, fifth and tenth minutes as routinely given after delivery by healthcare providers were documented; as well as data on neonates who had altered tone and/or clinically apparent seizures within the first 24 hours of life.

Counts and proportions were used to summarise categorical data while median and interquartile range were used to summarise continuous variables. The chi squared test (or Fisher’s exact test if any expected cell count was <5) was used to assess significant differences in categorical variables across asphyxia and no asphyxia groups. The Wilcoxon rank sum test was used to test association between predictors and outcomes for continuous variables. Effective APGAR score use was computed as sensitivity, specificity, positive and negative predictive values. Intraclass correlations did not identify the need for multi-level regression models in this study; thus, one-level logistic regression was used at a 95% confidence level to determine independent factors associated with ineffective APGAR score use, with the dependent variable being incorrect APGAR scores.

This study received ethical approval from the Institutional Review and Ethics Committee of Moi Teaching and Referral Hospital / Moi University School of Medicine (Approval 0003781). Additionally, an administrative approval was obtained from the Chief Executive Officer (CEO) of Moi Teaching and Referral Hospital (Ref. ELD/MTRH/R&P/10/2/V.2/2010), and a research permit was gotten from the National Commission for Science, Technology, and Innovation Kenya (Ref. 791482). Prior to enrolment of neonates, a written informed consent was obtained from the parents of neonates who met eligibility to participate in this study. Furthermore, healthcare workers provided a written informed consent before partaking in this study.

 Results

This study enrolled 102 neonates, of whom, slightly more than half were male, 52 (51%). The median [IQR] birth weight and gestational age were 3,010g [IQR: 2,752, 3,375] and 39.0 [IQR: 37.0, 40.2] weeks respectively. About two-thirds of the neonates, 65 (63.7%), were born via spontaneous vaginal delivery. Labour was induced in 11 deliveries (10.8%), with the most frequent indication being premature rupture of membranes (5 [45.5%]), seconded by postdate pregnancies (4 [36.4%]). The median [IQR] APGAR score at the 5th minute was 9.0 [IQR: 8.0, 10.0], and 24 (23.5%) neonates were observed to have an APGAR score of <7 at this 5th minute. The median [IQR] cord blood pH at birth was 7.20 [7.09, 7.29] and 7.20 [7.13, 7.28] at the 5th minute. Eleven neonates (10.8%) had clinically apparent seizures, while 17 (16.7%) were noted to have altered tone (Table 1).

10.1371/journal.pone.0285828.t001 Neonatal sociodemographic and clinical characteristics.
Characteristic Overall, N = 102 No asphyxia, N = 81 Asphyxia1, N = 21 p-value2
Sex of the neonate, n (%) 0.04
    Female 50.0 (49.0) 44.0 (54.3) 6.0 (28.6)
    Male 52.0 (51.0) 37.0 (45.7) 15.0 (71.4)
Weight (g), median [IQR] 3,010 [2,752, 3,375] 3,015 [2,795, 3,320] 3,000 [2,620, 3,500] 0.82
Gestational age (months), median [IQR] 39.0 [37.0, 40.2] 39.0 [37.0, 40.1] 39.5 [38.0, 41.0] 0.20
Induction of labour, n (%) 11.0 (10.8) 7.0 (8.6) 4.0 (19.0) 0.23
1 Indication for induction of labour, n (%) 0.27
    Post date 4.0 (36.4) 3.0 (42.9) 1.0 (25.0)
    PROM 5.0 (45.5) 4.0 (57.1) 1.0 (25.0)
    SPET 2.0 (18.2) 0.0 (0.0) 2.0 (50.0)
Method of delivery, n (%) 0.014
    Caesarean section (CS) 34.0 (33.3) 28.0 (34.6) 6.0 (28.6)
    Instrumental vaginal delivery (IVD) 3.0 (2.9) 0.0 (0.0) 3.0 (14.3)
    Normal vaginal delivery 65.0 (63.7) 53.0 (65.4) 12.0 (57.1)
APGAR score at birth
Median [IQR] 8.0 [7.3, 9.0] 9.0 [8.0, 9.0] 7.0 [6.0, 7.0] <0.001
APGAR score < 7, n (%) 26.0 (25.5) 10.0 (12.3) 16.0 (76.2) <0.001
5th minute APGAR score
Median [IQR] 9.0 [8.0, 10.0] 9.0 [9.0, 10.0] 7.0 [6.0, 8.0] <0.001
APGAR score < 7, n (%) 24.0 (23.5) 9.0 (11.1) 15.0 (71.4) <0.001
10th minute APGAR score
Median [IQR] 10.0 [9.0, 10.0] 10.0 [10.0, 10.0] 8.0 [8.0, 10.0] <0.001
APGAR score < 7, n (%) 6.0 (5.9) 2.0 (2.5) 4.0 (19.0) 0.016
Cord blood pH at birth, median [IQR] 7.20 [7.09, 7.29] 7.23 [7.14, 7.32] 7.00 [6.97, 7.00] <0.001
Cord blood pH at the 5th minute, median [IQR] 7.20 [7.13, 7.28] 7.21 [7.15, 7.30] 7.12 [7.06, 7.16] <0.001
Clinically apparent seizures, n (%) 11.0 (10.8) 0.0 (0.0) 11.0 (52.4) <0.001
Altered tone, n (%) 17.0 (16.7) 0.0 (0.0) 17.0 (81.0) <0.001

1 Amongst the 11 babies born post induced labour.

2 p values from Wilcoxon rank sum test, Fisher’s exact test, and Pearson’s Chi-squared test as appropriate.

Among all the 102 neonates enrolled, 21 (21%) had birth asphyxia defined as cord blood pH at birth <7 and presence of clinically apparent seizures and/or an altered tone. The median [IQR] APGAR score was significantly lower amongst neonates with birth asphyxia compared to neonates without birth asphyxia (p <0.001) at birth (7.0 [IQR: 6.0, 7.0] vs. 9.0 [IQR: 8.0, 9.0]), at the 5th minute (7.0 [IQR: 6.0, 8.0] vs. 9.0 [IQR: 9.0, 10.0]), and at the 10th minute (8.0 [IQR: 8.0, 10.0] vs. 10.0 [IQR: 10.0, 10.0])–Fig 2.

10.1371/journal.pone.0285828.g002 Violin plots showing the distribution of APGAR score at various time points by birth asphyxia status.

A total of 64 healthcare workers assigned APGAR scores to the 102 neonates. The median [IQR] age of the healthcare providers was 34.5 [31.0, 37.0] years and 40 (63%) were female. Of these healthcare workers, there were 13 (20%) students, 3 (5%) medical officers, 31 (49%) midwives, 13 (20%) paediatric residents, and 4 (6%) paediatric consultants. Half (50%) of the healthcare providers had between five- and ten-years working experience with the minimum (2%) observed to have worked for more than 15 years (Table 2).

10.1371/journal.pone.0285828.t002 Socio-demographic characteristics of the healthcare providers who scored the neonates.
Characteristic Total, N = 64
Age (years), median [IQR] 34.5 [31.0, 37.0]
Sex, n (%)
    Female 40.0 (62.5%)
    Male 24.0 (37.5%)
Cadre, n (%)
    Medical officer 3.0 (4.7%)
    Midwife 31.0 (48.5%)
    Paediatric consultant 4.0 (6.2%)
    Paediatric resident 13.0 (20.3%)
    Student 13.0 (20.3%)
1Education, n (%)
    Diploma 14.0 (45.2%)
    Higher National Diploma 4.0 (12.9%)
    Bachelor’s degree 12.0 (38.7%)
    Master’s degree 1.0 (3.2%)
Years of work experience, n (%)
    <5 years 20.0 (31.3%)
    5–10 years 32.0 (50.0%)
    >10–15 years 11.0 (17.2%)
    >15 years 1.0 (1.6%)

1Amongst midwives.

Healthcare providers agreed to considering the following when assigning APGAR scores: 59 (92%) consider the individual parameters of the score, 45 (70%) seek a second opinion before assigning scores and 47 (73%) routinely consider the second opinions, 57 (89%) consider the need for resuscitation, 54 (84%) consider the nature of the resuscitation, 46 (72%) consider the duration of the resuscitation, 32 (50%) consider the time of the day, and 42 (66%) typically consider the type of delivery. Fifty-one (80%) reported having ready access to the APGAR scoring chart; however, only 24 (38%) felt the need to refer to the APGAR scoring chart before assigning a score to a neonate.

Table 3A is a 2 x 2 table of birth asphyxia as diagnosed by an assigned APGAR score of <7 at the 5th minute versus birth asphyxia as diagnosed by a cord blood pH of <7 at birth with the presence of clinically apparent seizures and/or an altered tone (gold standard).

10.1371/journal.pone.0285828.t003 a: Diagnosis of birth asphyxia using APGAR score at the 5th minute versus cord pH at birth.

b: APGAR scoring at the 5th minute for the diagnosis of birth asphyxia.

Cord pH at birth with clinically apparent seizures and/or altered tone
Asphyxia No asphyxia Total
APGAR score at the 5th minute Asphyxia 15 (True Positives) 9 (False Positives) 24
No asphyxia 6 (False Negatives) 72 (True Negatives) 78
Total 21 81 102
Parameter Value (95% CI)
Accuracy 0.85 (0.77, 0.92)
Sensitivity 0.71 (0.48, 0.89)
Specificity 0.89 (0.80, 0.95)
Positive predictive value 0.62 (0.41, 0.81)
Negative predictive value 0.92 (0.84, 0.97)
Positive likelihood ratio 6.43 (3.28, 12.60)
Negative likelihood ratio 0.32 (0.16, 0.63)

Of the neonates with birth asphyxia, 15 were truly identified by APGAR scoring at the 5th as having birth asphyxia (sensitivity: 0.71 [95% CI: 0.48, 0.89]), and of the neonates without birth asphyxia, 72 were truly identified by APGAR scoring at the 5th minute as not having birth asphyxia (specificity: 0.89 [95% CI: 0.80, 0.95]) as shown on Table 3B.

Neonates born via instrumental vaginal delivery had 8.83 times higher odds (95% CI: 0.79, 199) of having an incorrect asphyxia classification compared to neonates born via normal vaginal delivery. In resuscitated neonates, there was a 23.83 (6.72, 101.99) times significantly higher odds of an incorrect asphyxia classification; however, the nature of resuscitation done was not a statistically significant finding. Healthcare practitioners without access to an APGAR scoring chart were significantly more likely (OR: 56.0 [95% CI: 12.9, 322.3]) to incorrectly classify asphyxia compared to healthcare practitioners with access to an APGAR scoring chart. Neonate-related factors (sex, and birth weight) were controlled for in the logistic regression analysis as shown on Table 4.

10.1371/journal.pone.0285828.t004 Factors associated with an incorrect asphyxia classification based on APGAR scoring.
Variable OR (95% CI) p value 1 aOR (95% CI) p value
Neonate related factors
    Sex (Female) 0.89 (0.29, 2.70) 0.84 0.85 (0.27, 2.62) 0.78
    Birth weight 0.99 (0.99, 1.00) 0.73 1.00 (0.99, 1.00) 0.88
Healthcare practitioner related factors
    Age (in years) 1.06 (0.95, 1.20) 0.35 1.06 (0.95, 1.20) 0.32
    Sex (Female) 0.60 (0.20, 1.87) 0.38 0.86 (0.19, 1.81) 0.34
Cadre 0.74 0.35
    Student Ref. - Ref. -
    Midwife 1.75 (0.38, 12.41) 0.51 2.34 (0.49, 17.08) 0.33
    Medical officer 2.75 (0.11, 36.59) 0.45 1.05 (0.34, 223.03) 0.13
    Paediatric resident 3.38 (0.58, 26.96) 0.19 6.87 (0.98, 65.03) 0.06
    Paediatric consultant 2.75 (0.11, 36.59) 0.45 7.09 (0.25, 124.4) 0.18
Education level (midwives only) 0.45 0.49
    Diploma Ref. - Ref. -
    Higher National Diploma 0.51 (0.16, 1.72) 0.26 0.53 (0.16, 1.83) 0.30
    Bachelor’s degree 0.19 (0.01, 1.24) 0.14 0.19 (0.01, 1.34) 0.15
    Master’s degree - - - -
Years of experience 0.75 0.77
    <5 years Ref. - Ref. -
    5–10 years 0.29 (0.01, 1.92) 0.27 0.31 (0.02, 2.2) 0.31
    >10–15 years - -
    >15 years 0.89 (0.28, 2.96) 0.84 0.99 (0.30, 3.43) 0.98
Method of delivery 0.03 0.04
    Normal vaginal delivery Ref. - Ref. -
    Caesarean section (CS) 0.13 (0.01, 0.73) 0.05 0.12 (0.01, 0.77) 0.06
    Instrumental vaginal delivery (IVD) 8.83 (0.79, 199) 0.08 9.87 (0.81, 236) 0.08
Individual APGAR score parameters 0.41 (0.02, 2.31) 0.27 0.42 (0.02, 2.45) 0.43
The need for resuscitation 23.83 (6.72, 101.99) <0.001 27.82 (7.29, 134.80) <0.001
Nature of resuscitation 0.99 0.98
     Suctioning/stimulation Ref. - Ref. -
    Bag/mask ventilation 1.00 (0.07, 13.85) 1.00 0.67 (0.01, 12.4) 0.78
    Chest compressions 0.00 (-, -) 0.99 0.99
    Intubation 0.00 (-, -) 0.99 0.99
    Oxygenation 0.67 (0.04, 10.03) 0.77 0.35 (0.01, 7.22) 0.52
    Use of adrenaline 0.00 (-, -) 0.99 0.99
Lack of access to APGAR score chart 56.0 (12.9, 322.3) <0.001 78.9 (15.5, 661.7) <0.001

1Odds ratio adjusted for gestational age, sex of the neonate, and the birth weight of the neonate, one-level logistic regression analysis.

 Discussion Effective use of the APGAR score

We estimated a sensitivity of 71% and a specificity of 89%. Our specificity was more comparable to that of a study prospective cohort study conducted among 464 neonates admitted to a tertiary hospital in Iran at 81% [11]. On the other hand, we had a lower sensitivity of 71% compared to the 81% in Iran [11].

We postulate that, our low sensitivity can be explained by a form of ascertainment bias, which is also in line with findings from a review on the APGAR score by the score’s founder, Dr. Virginia Apgar. She recommended in this review that, the person carrying out the delivery shouldn’t be the one assigning the APGAR score as they could have a vested interest in the neonatal outcome, and also have divided attention in view of the need for continual maternal management [9,29]. The practice for most deliveries in MTRH except caesarean deliveries is that the person carrying out the delivery also assigns the APGAR score to the neonate. This could have therefore resulted in incorrectly high APGAR scores, and true asphyxia being reported (per APGAR score) as no asphyxia, translating to low sensitivity. On the flip side, the scores observed in our study were better at determining babies who did not have birth asphyxia.

A multicenter study that assessed accuracy of the APGAR score and umbilical cord blood parameters in diagnosing birth asphyxia, reported an APGAR score sensitivity of 99% and a specificity of 41% [20]. These findings were dissimilar to ours in that, our sensitivity was lower at 71%, and our specificity was higher than theirs at 89%. The difference could be explained by the fact that in the multicenter study, APGAR scores in the first minute were used; while in our study, we used APGAR scores in the fifth minute in our operational definition for birth asphyxia. The use of fifth-minute APGAR scores in the current study was adopted from the combined consensus of the American College of Obstetricians and Gynecologists/American Academy of Pediatrics (ACOG/AAP).

We observed a positive predictive value of 0.62 and a negative predictive value of 0.92. Park and associates in their study reported a positive predictive value of 19.4 and a negative predictive value of 96.2 [19]. As clearly shown, our negative predictive values are comparable. On the other hand, they had a much lower positive predictive value when compared with ours. This difference could be explained by two things. Firstly, they applied the APGAR score in their study as a predictive tool for neonatal mortality, while we used it for diagnosis of asphyxia in our study. Secondly, they included extremely low birth weight babies in their study, and we did not.

 Healthcare provider factors affecting effective use of APGAR score

In the current study, mode of delivery, need for resuscitation and lack of access to an APGAR scoring chart were significantly associated with the effective use of the APGAR score.

Mode of delivery was significantly associated with incorrect APGAR scores whereby, babies born via instrumental deliveries were 8 times more likely to have incorrect scores when compared with neonates born via spontaneous vaginal delivery. Additionally, neonates born via caesarean deliveries were slightly less likely to be assigned incorrect scores with an odds ratio of 0.13. Our findings can be attributed to the concept of normalcy by which, deliveries requiring intervention are already viewed as a deviation from the norm—spontaneous vaginal deliveries, and thus have a beforehand expectation of poor neonatal outcome. Therefore, it is possible that this could have negatively influenced how effectively the APGAR score was used in deliveries requiring intervention in our study. This was however more applicable to instrumental deliveries than caesarean births in our study and we think it was so because, we included babies born via elective caesarean sections with healthy outcomes in which case, the assigning of APGAR scores is forthright. Our findings agreed to a previous study which reported that neonates born via normal vaginal deliveries were more likely to be better scored than their counterparts born through other methods of delivery [22].

Babies who underwent resuscitation in our study were 23.83 times more likely to be assigned incorrect APGAR scores. We presuppose that, this finding could be attributed to the conventional APGAR score itself, as it does not take into account neonatal resuscitation. Additionally, given that the person resuscitating is also the one who scores the neonate, there may have been an element of ascertainment bias whereby, some scores could have been assigned incorrectly to evade responsibility of negative neonatal outcomes. Our findings mirror those reported in another developing country where a significant variation was noted in the APGAR scores assigned to resuscitated versus non-resuscitated babies [27]; and those from a developed country, where the authors [30] observed great variability in the respiratory component of the APGAR score among healthcare providers in the context of resuscitation. Furthermore, in Richmond-Virginia [21], subjective APGAR scoring by healthcare providers in the setting of neonatal resuscitation was detected, leading the authors to recommend the use of other scores such as the Expanded APGAR score or Neonatal Resuscitation and Adaptive score to replace the conventional APGAR score in resuscitated babies. We also highlight this need for alternative scoring methods for resuscitated babies.

Healthcare practitioners without access to an APGAR scoring chart were significantly more likely to incorrectly classify asphyxia compared to healthcare practitioners with access to an APGAR scoring chart. We postulate that, having access to an APGAR scoring chart could have resulted in better utilization of the score in terms of more objective application of the score parameters, as opposed to attempting to apply the score off by heart without the score chart. Our findings were identical to those reported in Nigeria [31], a study carried out in a similar low-resource setting like the current study. Additionally, recommendations have been made regarding a review of the guidelines of the use of the APGAR score among healthcare providers [32].

 Conclusion and recommendations

This study reports low sensitivity and positive predictive values of assigned APGAR scores at 71% and 62% respectively among newborns attending a tertiary hospital in Western Kenya. Newborns who were resuscitated, born by instrumental deliveries, and assigned APGAR scores by healthcare providers without access to the APGAR scoring chart were significantly more likely to get incorrect APGAR scores. With the foregoing, there is need to adopt the gold-standard of birth asphyxia diagnosis into the hospital-based neonatal management guidelines at the tertiary hospital and other resource constrained healthcare settings. In addition, improved APGAR scoring is attainable by augmenting availability of APGAR scoring charts, continuous medical education programs on the score, and on neonatal resuscitation. Additional studies should be conducted to explore the applicability of other neonatal assessment scores for resuscitated neonates.

 Supporting information Supplementary Material 1: Data Collection Form (Maternal and Neonatal).

(DOCX)

 Supplementary Material 2: Data Collection Form (Healthcare Workers).

(DOCX)

 Supplementary Material 3: Standard Operating Procedure for Umbilical Cord Blood Collection.

(DOCX)

 Supplementary Material 4: Dataset.

(XLSX)

 References Wang H, Bhutta ZA, Coates MM, Coggeshall M, Dandona L, Diallo K, et al. Global, regional, national, and selected subnational levels of stillbirths, neonatal, infant, and under-5 mortality, 1980–2015: a systematic analysis for the Global Burden of Disease Study 2015. The Lancet. 2016 Oct 8;388(10053):1725–74. doi: 10.1016/S0140-6736(16)31575-6 27733285 UNICEF for every child. Child Mortality [Internet]. UNICEF DATA. 2021 [cited 2022 Sep 4]. Available from: https://data.unicef.org/topic/child-survival/under-five-mortality/. Yelamali B, Panigatti P, Pol R, Talawar K, Naik S, Badakali A. Outcome of newborn with birth asphyxia in tertiary care hospital—a retrospective study. 2014;6. Arunda M, Emmelin A, Asamoah BO. Effectiveness of antenatal care services in reducing neonatal mortality in Kenya: analysis of national survey data. Global Health Action. 2017 May 13;10(1):1328796. doi: 10.1080/16549716.2017.1328796 28621201 KDHS. Kenya Demographic and Health Survey 2014. Central Bureau of Statistics (CBS) [Kenya] Kenya Demographic and Health Survey. 2014; iii–372. Lambon-Quayefio MP, Owoo NS. Examining the Influence of Antenatal Care Visits and Skilled Delivery on Neonatal Deaths in Ghana. Applied Health Economics and Health Policy. 2014 May 13;12(5):511–22. doi: 10.1007/s40258-014-0103-z 24934923 Halim A, Dewez JE, Biswas A, Rahman F, White S, van den Broek N. When, Where, and Why Are Babies Dying? Neonatal Death Surveillance and Review in Bangladesh. PLoS ONE. 2016 May 13;11(8). doi: 10.1371/journal.pone.0159388 27478900 Organization WH. Every newborn: an action plan to end preventable deaths. Geneva: World Health Organization; 2014. Sabol BA, Caughey AB. Acidemia in neonates with a 5-minute Apgar score of 7 or greater–What are the outcomes? American Journal of Obstetrics and Gynecology. 2016 Mar 29;215(4): 486.e1-486.e6. Rüdiger M, Braun N, Aranda J, Aguar M, Bergert R, Bystricka A, et al. Neonatal assessment in the delivery room—Trial to Evaluate a Specified Type of Apgar (TEST-Apgar). BMC pediatrics. 2015; 15:18. doi: 10.1186/s12887-015-0334-7 25884954 Dalili H, Nili F, Sheikh M, Hardani AK, Shariat M, Nayeri F. Comparison of the Four Proposed Apgar Scoring Systems in the Assessment of Birth Asphyxia and Adverse Early Neurologic Outcomes. Weitkamp JH, editor. PLOS ONE. 2015 Mar 29;10(3): e0122116. doi: 10.1371/journal.pone.0122116 25811904 Wayenberg JL, Vermeylen D, Bormans J, Magrez P, Müller MF, Pardou A. Diagnosis of severe birth asphyxia and early prediction of neonatal neurological outcome in term asphyxiated newborns. Journal of Perinatal Medicine. 1994;22(2):129–36. doi: 10.1515/jpme.1994.22.2.129 7965542 American Academy of Pediatrics AA of. Neonatal Encephalopathy and Neurologic Outcome, Second Edition Report of the American College of Obstetricians and Gynecologists’ Task Force on Neonatal Encephalopathy. Pediatrics. 2014 Apr 9;133(5): e1482–8. Fares K, Mehdi HA, Imad BM. Correlation between Umbilical Cord pH, Apgar Score and Pregnancy Outcome in High-Risk Pregnancy. 2019;7(2):5. American Academy of Pediatrics C on F and N. The Apgar Score | Pediatrics | American Academy of Pediatrics [Internet]. 2015 [cited 2022 Sep 4]. Available from: https://publications.aap.org/pediatrics/article/136/4/819/73821/The-Apgar-Score?autologincheck=redirected?nfToken=00000000-0000-0000-0000-000000000000. Department of Pediatrics Rajah Muthiah Medical College, Chidambaram Kiruthiga DG. Prediction of Neonatal Seizures in HIE by APGAR Score and Umbilical Cord Blood pH. jmscr [Internet]. 2018 Apr 3 [cited 2020 Apr 9];6(4). Available from: http://jmscr.igmpublication.org/v6-i4/17%20jmscr.pdf. Pathak V, Sahu DS. Relation between immediate postpartum APGAR score with umblical cord blood pH and fetal distress. In 2019. Admasu FT, Melese BD, Amare TJ, Zewude EA, Denku CY, Dejenie TA. The magnitude of neonatal asphyxia and its associated factors among newborns in public hospitals of North Gondar Zone, Northwest Ethiopia: A cross-sectional study. PLoS One. 2022 Mar 4;17(3): e0264816. doi: 10.1371/journal.pone.0264816 35245309 Park JH, Chang YS, Ahn SY, Sung SI, Park WS. Predicting mortality in extremely low birth weight infants: Comparison between gestational age, birth weight, Apgar score, CRIB II score, initial and lowest serum albumin levels. PLOS ONE. 2018 Dec 3;13(2): e0192232. doi: 10.1371/journal.pone.0192232 29438382 Parameters CSG of NUCBG. [Multicenter clinical study on umbilical cord arterial blood gas parameters for diagnosis of neonatal asphyxia]. Zhonghua Er Ke Za Zhi = Chinese Journal of Pediatrics. 2010;48(9):668–73. 21092525 Jurdi SR, Jayaram A, Sima AP, Hendricks Muñoz KD. Evaluation of a Comprehensive Delivery Room Neonatal Resuscitation and Adaptation Score (NRAS) Compared to the Apgar Score: A Pilot Study. Global Pediatric Health. 2015 Oct 6; 2:2333794X15598293. Kostro M, Jacyna N, Głuszczak-Idziakowska E, Sułek-Kamas K, Jakiel G, Wilińska M. Factors affecting the differentiation of the Apgar score and the biochemical correlation of fetal well-being—a prospective observational clinical study. Developmental period medicine. 2018; 22:238–46. doi: 10.34763/devperiodmed.20182203.238246 30281519 Simon L V, Hashmi MF, Bragg BN. APGAR Score. In: StatPearls. Treasure Island (FL): StatPearls Publishing; 2020. Bang A, Patel A, Bellad R, Gisore P, Goudar SS, Esamai F, et al. Helping Babies Breathe (HBB) training: What happens to knowledge and skills over time? BMC pregnancy and childbirth. 2016;16(1):364. doi: 10.1186/s12884-016-1141-3 27875999 Rule ARL, Maina E, Cheruiyot D, Mueri P, Simmons JM, Kamath-Rayne BD. Using quality improvement to decrease birth asphyxia rates after “Helping Babies Breathe” training in Kenya. Acta Paediatrica (Oslo, Norway: 1992). 2017;106(10):1666–73. doi: 10.1111/apa.13940 28580692 Hajian-Tilaki K. Sample size estimation in diagnostic test studies of biomedical informatics. Journal of Biomedical Informatics. 2014 Apr 1; 48:193–204. doi: 10.1016/j.jbi.2014.02.013 24582925 Chiabi A, Kago DA, Moyo GK, Obadeyi B. Relevance and Applicability of the Apgar Score in Current Clinical Practice. 2019;7. Jung E, Romero R, Yeo L, Diaz-Primera R, Marin-Concha J, Para R, et al. The fetal inflammatory response syndrome: the origins of a concept, pathophysiology, diagnosis, and obstetrical implications. Seminars in Fetal and Neonatal Medicine. 2020 Aug 1;25(4):101146. doi: 10.1016/j.siny.2020.101146 33164775 Apgar V. The newborn (Apgar) scoring system. Reflections and advice. Pediatric clinics of North America. 1966. doi: 10.1016/s0031-3955(16)31874-0 5946299 Niemuth M, Küster H, Simma B, Rozycki H, Rüdiger M, European Society for Paediatric Research (ESPR) Neonatal Resuscitation Section Writing Group, et al. A critical appraisal of tools for delivery room assessment of the newborn infant. Pediatr Res. 2021 Dec 30. Mukhtar-Yola M, Audu LI, Olaniyan O, Akinbi HT, Dawodu A, Donovan EF. Decreasing birth asphyxia: utility of statistical process control in a low-resource setting. BMJ Open Quality. 2018 Dec 3;7(3): e000231. doi: 10.1136/bmjoq-2017-000231 30234170 Simon LV, Hashmi MF, Bragg BN. APGAR Score. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2020 [cited 2020 Apr 7]. Available from: http://www.ncbi.nlm.nih.gov/books/NBK470569/. 10.1371/journal.pone.0285828.r001 Decision Letter 0 Olorunfemi Gbenga Academic Editor 2023 Gbenga Olorunfemi This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Submission Version 0

21 Nov 2022

PONE-D-22-21860Assessment of effective use of APGAR score in comparison to the gold standard in diagnosis of birth asphyxia at Moi Teaching and Referral Hospital, Kenya.PLOS ONE

Dear Dr. Njie,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

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ACADEMIC EDITOR:We suggest that authors make their anonymous data supporting the work to be publicly available unless there is any restriction which should be explicitly stated.

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Academic Editor

PLOS ONE

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Reviewer #1: Yes

Reviewer #2: Yes

**********

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Reviewer #1: Yes

Reviewer #2: Yes

**********

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Reviewer #1: Yes

Reviewer #2: Yes

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Reviewer #2: No

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Reviewer #1: The article is technically and scientifically sound. The only suggested typo identified was the concomitant use of "<" "less than". The article was well written. The style of writing, the language and the soundness of the article is commendable.

Reviewer #2: General comment: Consider employing Professional English Language editing services for this manuscript.

Title: Consider modifying the title to ' A comparative analysis of APGAR score and the gold standard in the diagnosis of birth asphyxia at a tertiary health facility in Kenya.

Short title: Expunge repeated phrase 'compared to'

Line 66-69: A synonymous phrase for neonatality mortality like 'neonatal death' can be used.

Line 84- Major cause or contributor

Line 87 - Consider using a linking word for clarity.

Methods: How were the participants recruited? How did the authors arrive at the total number of participants to be used (sample size)? Consider using a flow chart for these aspects.

Results- 64% is not majority, it's about two-thirds

line 217,234-240 should be rephrased

There should be a consistent use of decimal points in the tables.

Discussion: lines 216-219 have previously been discussed in the abstract and introduction.

Line 224-225- This should be in the conclusion and recommendation

References - Most references used are over 10 years old. Aren't there are more recent articles on the subject matter?

**********

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Reviewer #1: Yes: M.A.N. ADEBOYE

Reviewer #2: No

**********

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Submitted filename: MAN ADEBOYE EDITED PONE-D-22-21860.pdf

 10.1371/journal.pone.0285828.r002 Author response to Decision Letter 0 Submission Version 1

24 Jan 2023

I have cited Tables 2 and 4 in the text.

Submitted filename: Response to Reviewers.docx

 10.1371/journal.pone.0285828.r003 Decision Letter 1 Olorunfemi Gbenga Academic Editor 2023 Gbenga Olorunfemi This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Submission Version 1

28 Mar 2023

PONE-D-22-21860R1A comparative analysis of APGAR score and the gold standard in the diagnosis of birth asphyxia at a tertiary health facility in Kenya.PLOS ONE

Dear Dr. Njie,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

Please submit your revised manuscript by May 12 2023 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

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An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: https://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols.

We look forward to receiving your revised manuscript.

Kind regards,

Gbenga Olorunfemi, MBBS,MSC,FMCOG,FWASC

Academic Editor

PLOS ONE

Journal Requirements:

Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

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Comments to the Author

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Reviewer #2: All comments have been addressed

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #2: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #2: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #2: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #2: Yes

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #2: Dear author, consider the following minor corrections.

Line 133: Methods: Rephrase to interviewer-administered, not interviewer-filled

Line 165: Result: 51% is approximately half, not majority. Consider rephrasing that.

**********

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Reviewer #2: No

**********

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 10.1371/journal.pone.0285828.r004 Author response to Decision Letter 1 Submission Version 2

29 Apr 2023

I would like to submit corrections for my manuscript entitled "Assessment of effective use of APGAR score in comparison to the gold standard in diagnosis of birth asphyxia at Moi Teaching and Referral Hospital, Kenya."

Reviewer #2: Dear author, consider the following minor corrections.

Comment 1: Line 133: Methods: Rephrase to interviewer-administered, not interviewer-filled.

Response to Comments 1: The methods section (now Line 131) has been rephrased to “Interviewer-administered semi-structured questionnaires”.

Comment 2: Line 165: Result: 51% is approximately half, not majority. Consider rephrasing that.

The results section (now Line 163) has been rephrased to “slightly more than half were male, 52 (51%)”.

Yours faithfully,

Corresponding Author,

Dr. Njie Albertine.

Submitted filename: Response to Reviewers 29042023.docx

 10.1371/journal.pone.0285828.r005 Decision Letter 2 Olorunfemi Gbenga Academic Editor 2023 Gbenga Olorunfemi This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Submission Version 2

3 May 2023

A comparative analysis of APGAR score and the gold standard in the diagnosis of birth asphyxia at a tertiary health facility in Kenya.

PONE-D-22-21860R2

Dear Dr. Njie,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

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Kind regards,

Gbenga Olorunfemi, MBBS,MSC,FMCOG,FWASC

Academic Editor

PLOS ONE

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