Patterns of Acute Bilirubin Encephalopathy in Nigeria: A Multicenter Pre-Intervention Study

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Journal of Perinatology

https://doi.org/10.1038/s41372-018-0094-y

ARTICLE

Patterns of acute bilirubin encephalopathy in Nigeria: a multicenter


pre-intervention study
Udochukwu M Diala 1 Richard P Wennberg2 Isa Abdulkadir3 Zubaida L Farouk 4 Carlos D. Coda Zabetta5
● ● ● ● ●

Efe Omoyibo6 Abieyuwa Emokpae7 Aleksandr Aravkin8 Bose Toma1 Stephen Oguche1
● ● ● ● ●

Tina Slusher9 *On behalf of the Stop Kernicterus In Nigeria (SKIN) study group

Received: 21 October 2017 / Revised: 16 January 2018 / Accepted: 26 February 2018


© Nature America, Inc., part of Springer Nature 2018

Abstract
Background Acute bilirubin encephalopathy (ABE) is an important cause of neonatal morbidity in Nigeria, accounting for
5–14% of neonatal deaths. Most newborns with severe ABE have irreversible damage before receiving treatment empha-
sizing the need for timely pre-admission monitoring and referral. There is limited evidence that educational interventions
targeting mothers and health care providers will reduce delayed care.
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Objective To provide baseline data on the incidence of ABE and associated pre-admission risk factors in five centers of
Nigeria in order to evaluate the effect of subsequent educational interventions on outcome.
Study design The incidence of ABE among newborns treated for hyperbilirubinemia was documented prospectively.
Bivariate analysis and multivariate logistic regression were used to evaluate risk factors for acute bilirubin encephalopathy
and reasons for regional differences in its occurrence.
Results Of 1040 infants, 159 treated for hyperbilirubinemia (15.3%) had mild to severe bilirubin encephalopathy (including
35 deaths), but the incidence ranged from 7 to 22% between centers. Logistic regression identified four common predictors:
total serum bilirubin (odds ratio 1.007 per mg/dl rise), out-of-hospital births (OR 2.6), non-alloimmune hemolytic anemia
(OR 2.8), and delayed care seeking (OR 4.3).
Conclusion The high occurrence of bilirubin encephalopathy in Nigeria is due in large part to a delay in seeking care. A
planned intervention strategy will target conditions leading to severe hyperbilirubinemia and delay.

Electronic supplementary material The online version of this article


(https://doi.org/10.1038/s41372-018-0094-y) contains supplementary
Background
material, which is available to authorized users.
Acute bilirubin encephalopathy (ABE) is a major cause of
* Udochukwu M Diala mortality and morbidity in Nigeria, reported to occur in
[email protected]
[email protected]
2.2–3.4% of special care nursery admissions [1–3], and
account for 5–14% or more of neonatal deaths [4–7]. For
1
University of Jos, Jos, Nigeria every newborn that dies, 2–3 will have lifelong neurological
2
Department of Pediatrics, University of Washington, Seattle, WA, deficits ranging from auditory neuropathy spectrum disorder
USA to severe cerebral palsy [8–10]. In Nigeria, chronic bilirubin
3
Ahmadu Bello University, Zaria, Nigeria encephalopathy is a leading cause of cerebral palsy [11–13].
4 Most neonates with severe ABE have irreversible brain
Aminu Kano Teaching Hospital, Bayero University, Kano, Nigeria
5
injury before being admitted to treatment centers [14–16].
Bilimetrix s.r.l., Trieste, Italy
Thus, avoiding behaviors that promote hyperbilirubinemia
6
Federal Medical Centre, Asaba, Nigeria and delayed care seeking are critical. Educating health
7
Massey Street Children’s Hospital, Lagos, Nigeria providers and parents about dangers of jaundice and the
8
Department of Applied Mathematics, University of Washington, need for early evaluation has been recommended by several
Seattle, WA, USA investigators [17–22], but evidence that jaundice instruction
9
University of Minnesota and Hennepin County Medical Center, actually prevents ABE is limited. To that end, investigators
Minneapolis, MN, USA from five centers in Nigeria developed consensus programs
U. M. Diala et al.

for training physicians, nurses, midwives, clinical health “kernicteric facies” [23–26]. A diagnosis of ABE/suspected
extension workers (CHEWs), traditional birth attendants sepsis required signs consistent with both sepsis and ABE
(TBAs), and mothers (during antenatal and postpartum including fever/and or shock. An experienced attending
clinic visits) about risks for and management of neonatal physician confirmed all diagnoses of ABE. Secondary
jaundice. This report provides base-line data on the inci- outcomes were the number of patients admitted with a total
dence of severe hyperbilirubinemia and ABE among new- serum bilirubin (TSB) ≥20 mg/dL (342 µmol/L), a historic
borns treated for jaundice at each participating center and threshold for intervention [27], and TSB ≥30 mg/dL (513
examines demographic, behavioral and medical risk factors µmol/L), a threshold associated with high risk for ABE and
that contribute to regional differences in ABE occurrence. kernicterus [8, 28]. A delay in seeking/receiving care was
defined as an admisssion TSB ≥18 mg/dL in patients
admitted at 2 or more days of age; this represents a TSB
Methods greater than the 95th percentile at any age during the first
week of life [29].
Study sites
Laboratory data
The study involved nine major hospitals in five cosmopo-
litan cities in Nigeria representing varied urban densities, TSB was measured in hospital laboratories or contract pri-
ethnicity, language, culture and religious backgrounds. vate laboratories by colorimetric methods. ABO and Rh
Urban populations ranged from 174,000 in Asaba to over typing was performed for 830/1029 (81%) mother/infant
13 million inhabitants in Lagos (Supplement Table 1). pairs. Although planned, we G6PD screening was not
Asaba and Lagos are located in Southern Nigeria, Jos in obtained due to lack of funding and availability in partici-
Central and Zaria and Kano in Northern Nigeria. Yoruba pating centers. A diagnosis of severe hemolytic disease
and Igbo were predominant ethnic groups in the south and (SHD) was defined arbitrarily as a TSB level ≥20 mg/dl in a
Hausa in the north. All participants were treated with pho- patient with a hematocrit ≤35%.
totherapy and exchange transfusion when indicated. Inten-
sive phototherapy (irradiance ≥30 µW/cm2) was not Data collection
available at most study sites. Unfortunately, the study was
interrupted by strikes at federal and state funded hospitals Demographic and behavioral information was obtained
for several months limiting the total observation period from mothers at admission, to which were added laboratory
from a planned 13 months (65 center-months) to approxi- data and outcome observations (supplement Table 2).
mately 43 center-months.
Ethical considerations
Subject recruitment
Ethics Review Boards of each participating hospital
A total of 1106 newborns were treated for jaundice between approved the study. Verbal consent was obtained from
February 2014 and June 2015 of which 1040 were eligible mothers during admission interview. Patient identifiers were
for inclusion into the study after excluding patients with erased from data files following quality review and prior to
undocumented outcomes, deaths from unrelated causes, or final analysis. The study is registered with ClinicalTrials.
weighing <1000 g (averaging ~26 cases per center-month). gov, number NCT02713464.

Study design Statistical analysis

This was a pre-intervention prospective longitudinal Nominal data were compared using odds ratios and Pearson
hospital-based observational study documenting the inci- χ2 test. Statistical significance was defined as 0.05. Ordinal
dence of ABE and associated risk factors among patients data (TSB, age at admission, weight, mother’s age) were
treated for hyperbilirubinemia in participating centers. The bifurcated for paired analysis except in the logistic regres-
primary outcome was the presence of ABE, subdivided into sion model. Model selection for logistic regression was
mild (often reversible), moderate/severe ABE, death from performed using a weighted sum logistic regression of all
ABE, or ABE/suspect sepsis (usually lethal). Signs indica- variables and elastic net regulariazation [30] using an R
tive of mild ABE were lethargy, poor feeding, mild hypo- package general logistic model, GLMNET. This combines
tonia/hypertonia or high-pitched cry. Moderate/severe ABE rigid regularization [31] and the Lasso estimator [32] to
required the presence of opisthotonus, retrocollis, paralysis discover the most important predictors as well as correlation
of upward gaze, rigidity or flaccidity, apnea, seizures, or between groups of predictors of ABE. We then fit a
Patterns of acute bilirubin encephalopathy in Nigeria: a multicenter pre-intervention study

standard multiple logistic regression using the selected health provider referral) and delayed care seeking were
variables. highly correlated with ABE.
The most common behavior associated with ABE, irre-
spective of birth site or underlying pathology, was a delay
Results in seeking/receiving care (TSB > 95th percentile for age)
until severe hyperbilirubinemia or clinical signs of ABE
Subject characteristics appeared. The most common reason offered for delayed
care seeking was a failure to recognize the severity of
A total of 1040 patients were studied. Median admission jaundice (316/379 cases; 83%). Other reasons included
weight was 2700 g; 133 newborns weighed less than 2 kg. advice from family members and health care workers (e.g.,
The median admission age was 5 days; 132 patients were sun exposure, failed herbal trials) and transportation
admitted at birth or within 24 h of age and 82 were admitted problems.
at an age ≥10 days. The male/female ratio was 1.47. ABE trended higher with low birth weight, but the
magnitude of effect was surprisingly small and not sig-
Incidence of ABE and associated demographic/ nificant (P = .07). Male/female admission ratio was 1.5, but
behavioral risk factors ABE rates per admission were identical. Compared with
babies born to primigravid mothers, those born to multi-
159 cases of ABE were diagnosed among 1040 patients gravida mothers were more likely to be born outside of
admitted for treatment of jaundice (15.3%; Table 1). There hospitals (OR 1.97; 95% CI 1.44–2.67), have unskilled
were 35 ABE-related deaths yielding a case fatality rate of birth attendants and have a higher incidence of non-
22%. The average monthly occurrence was ~3.7 ABE alloimmune hemolytic anemia (OR 3.9; CI 1.73–8.70).
cases/center/month. A total of 176 patients were either However, despite these risks, delayed care seeking was only
inborn or admitted <2 days of age, and eight developed slightly higher among experienced mothers (OR 1.37; CI
ABE (4.7%; two with ABE/sepsis, five weighed ≤2 kg, and 1.01–1.88; P = 0.044), and the higher incidence of ABE
3/8 were outborn). Excluding these patients, the incidence (OR 1.48; CI 0.996–2.21) was not statistically significant.
of ABE among babies admitted for treatment when ≥2 days
of age increased from 15.3 to 17.3%. Eighty-three admis- Medical/laboratory associations with ABE
sions (8%) were 10 days of age or older; the median TSB
was 17.3 mg/dL, eight had TSB >30 mg/dL, and 8/83 had A total of 831/1040 infants (80%) had complete blood
ABE (9.6%). typing. Of these, 570/831 patients (69%) had no blood
Paired analyses of covariates associated with ABE, incompatibility, 64 of who had non-alloimmune SHD. TSB
reflecting the collective experience of all participating ≥30 mg/dl, ABO incompatibility, and SHD were highly
centers, are summarized in Table 2. Out-of-hospital births associated with ABE (P < 0.0001; Table 3). ABE occurred
(home plus clinic), births not attended by skilled worker in 55 of 190 (29%) newborns with TSB ranging 20–29.9
(physician or midwife), failure to have more than one mg/dL and in 61% of 107 infants with TSB ≥30 mg/dL. A
antenatal clinic visit, self-referral for care (compared with surprising 24% of patients with ABE had measured TSB
values <20 mg/dL. Twenty seven of the 35 patients with
low bilirubin ABE had one or more risk factors: weight
Table 1 Summary of major outcomes ≤2.5 kg (23; 11 weighed <2 kg), sepsis (2) and/or age at
admission ≥7 days of age (5). No known exposure to
Outcome N % ABE
bilirubin displacing agents was identified (e.g., salicylates)
Total patients studied 1029 but was not consistently asked.
Normal at discharge 872 SHD occurred in 99 patients including 5 of 38 patients
Total ABE 157 15.3% with Rh incompatibility, 24/226 infants with ABO incom-
Mild ABE 51 5.0% patibility, 63/577 babies with no maternal-infant blood type
Survived with ABE 71 6.9% incompatibility or sepsis, 5/204 with incomplete blood type
Died from ABE 23 2.2%
information and 2 newborns with ABE/sepsis. ABE
Died from ABE/sepsis 12 1.2%
occurred in 9 of 24 infants with SHD associated with ABO
incompatibility (38%), 36 of 63 infants (57%) with no
TSB ≥ 30 mg/dL–512 µmol/L (# ABE) 107 (65)a 6.4%
maternal/infant blood type compatibility and 2 of 5 infants
TSB ≥ 20–29.9 mg/dL (# ABE) 190 (55) 5.4%
with incomplete blood typing; G6PDd was suspected in
TSB < 20 mg/dL–342 µmol/L (# ABE) 721 (35) 3.4%
non-alloimmune cases, but enzyme activity was not
a
TSB was measured in 1018 patients. 2/11 without TSB had ABE measured.
U. M. Diala et al.

Table 2 Demographic/behavioral correlates with ABE: bivariate analysis


Pair Total ABE No ABE Odds OR 95% CI χ2 P value

Home birth 213 59 154 0.383 3.471 2.348–5.131 42.14 <0.0001


Hospital birth 684 68 616 0.110
Clinic birth 118 28 90 0.311 2.818 1.722–4.612 18.15 <0.0001
Hospital birth 684 68 616 0.110
Out of hospital 332 87 245 0.355 3.217 2.267–4.565 45.73 <0.0001
Hospital birth 684 68 616 0.110
Missing data 12 2 10
Delayed carea 379 132 247 0.534 16.17 9.275–28.21 146 <0.0001
No delay 469 15 454 0.033
Missing data 10 2 8
171 patients were admitted <2 days of age—8 developed ABE
Antenatal care
<2 clinic visits 101 30 71 0.423 2.754 1.720–4.410 18.97 <0.0001
≥ 2 clinic visits 842 112 730 0.153
Missing data 85 15 70
Birth attendant
Unskilled 229 60 169 0.355 2.572 1.785–3.705 26.95 <0.0001
MD/midwife 775 94 681 0.138
Missing data 25 3 22
Gravida 2+ 662 108 554 0.195 1.406 0.945–2.091 2.84 0.09
Gravida 1 312 38 274 0.139
Missing data 55 11 44
Self referral 427 78 349 0.224 2.874 1.582–5.218 12.91 <.001
Provider ref 194 14 180 0.078
Clinic ref 341 55 286 0.192 2.473 1.336–4.576 8.74 0.003
Missing data 67 10 57 (versus provider)
Male 610 90 520 0.173 0.946 0.668–1.340 0.1 0.75
Female 414 64 350 0.183
Missing data 5 3 2
Wt ≤ 2500 g 381 70 311 0.225 1.437 1.015–2.035 4.21 0.040
Wt > 2500 g 613 83 530 0.157
Missing data 35 4 31
CI confidence interval, ABE acute bilirubin encephalopathy, OR unadjusted odds ratio ref referral, wt weight on admission
a
Delayed care defined as presenting at care center with TSB ≥ 18 mg/dL after day 2 of life

Logistic regression
Table 3 Potential hematologic causes of hyperbilirubinemia and ABE
Etiology Cases ABE TSB ≥ 30 mg/dL Out of hospital delivery, non-alloimmune SHD, delay in
seeking care, and TSB level dominated all other risk con-
ABO incompatible 224 44 (20%) 31 (13.8%) ditions (Table 4, model A). Some highly correlated risk
Rhesus incompatible 37 1 (2.7%) 4 (10.8%) factors in bivariate analysis were reduced or disappeared in
Non-alloimune SHDa 64 38 (59%) 32 (50%) logistic regression because of the high interdependence of
No blood incompatibility 506 54 (10.7%) 28 (5.5%) many social/demographic variables. For example, the skill
Disease (hematocrit ≤ 35% in presence of severe hyperbilirubinemia of a birth attendant was not significant in any model that
(TSB ≥ 20 mg/dL) included birth site. However, with home birth excluded,
ABE acute bilirubin encephalopathy, TSB total serum bilirubin, SHD unskilled birth attendants emerged as critical factors
severe hemolytic (Table 4, model B), consistent with bivariate analysis; care
a
1/64 had ABE/sepsis provided by TBAs was associated with four times the risk
Patterns of acute bilirubin encephalopathy in Nigeria: a multicenter pre-intervention study

Table 4 Demographic/ behavioral correlates with ABE: logistic regression

A. Logistic regression model including birth site


Variable Odds ratio 95% Confidence interval P
≤1 antenatal clinic visit 2.0 (1.1, 3.6) 0.02
TSB (per mg/dL increase) 1.07 (1.04, 1.1) 1.0e-6
Non-alloimune hemolysis 2.8 (1.5, 5.3) 1.5e-3
Delay in receiving carea 4.3 (2.3, 8.1) 6.8e-6
Out of hospital birth 2.6 (1.7, 4.0) 2.1e-5
B. Logistic regression model including birth attendant
Variable Odds ratio 95% confidence interval P
≤1 antenatal clinic visit 2.3 (1.2, 4.3) 0.02
TSB (per mg/dL increase) 1.07 (1.04, 1.1) 1.0e-6
Non-alloimune hemolysis 2.9 (1.5, 5.3) 1.0e-3
Delay in receiving carea 4.5 (2.3, 8.5) 4.8e-6
b
Birth attendant: Midwife 1.7 (0.97, 3.0) 0.06
Birth attendant: TBA 4.2 (1.9, 9.5) 4.6e-4
Birth attendant: CHEW 3.8 (1.7, 8.3) 1.0e-3
Birth attendant family/none 1.7 (0.7, 4.2) 0.24
TBA traditional birth attendant, CHEW community health extension worker
a
Presenting at care center with TSB ≥ 18 mg/dL after day 2 of life
b
Compared with physician attended delivery

of developing ABE compared to physician attendance. collaborating centers in this study. In the vast majority of
Receiver Operating Characteristic analysis of ABE pre- cases, babies with advanced ABE were affected before
dictive models A and B had areas under the curve of 0.859 being admitted for care, in agreement with published
and 0.865 respectively (Figure 1, supplement). observations [14–16]. Four major risk factors for ABE were
identified in the population studied: severe hyperbilir-
Differences in incidence of ABE and ubinemia, hemolytic anemia, out-of-hospital birth, and
hyperbilirubinemia among centers delay in seeking/receiving care.
The relationship between elevated TSB and ABE is well
Participating centers had significant asymmetries in demo- established and occurred in 61% of newborns with TSB ≥30
graphic, social, and medical conditions as well as outcomes mg/dL. Studies from both Egypt [8] and United States [28]
(Table 3, supplement). The incidence of ABE per admission indicate that ABE and kernicterus is rare in term/near term
ranged from 7 to 22%. Major contributors to these differ- infants at TSB <30 mg/dL. Thus, the high number of ABE
ences were the rates of out-of-hospital births, non- cases occurring at TSB levels below 20 mg/dL was surprising
alloimmune hemolytic disease, antenatal care, and delay in but consistent with other reports from Nigeria. In a retro-
seeking or receiving care. The percentage of out-of-hospital spective study (2001–2006), Ogunlesi et al. [2], reported that
births ranged from 3.7% in Asaba to 58% in Kano. Kano and ABE occurred at TSB <20 mg/dL in 44 of 115 affected
Lagos had higher incidences of ABE and out-of-hospital newborns (38%), some of whom also had sepsis and/or
births, and fewer referrals from health providers than other prematurity. About half of affected babies with low TSB
centers (P < 0.001). Lagos had more cases of non- ABE in this study had either low birth weight, sepsis, or were
alloimmune SHD (40/63 total cases (P < 0.001). Among 33 admitted at >7 days age (suggesting that peak TSB was
babies with unexplained SHD and TSB ≥30 mg/dL, 18 were missed) [33]. The finding of ABE at low TSB in the absence
from Lagos. In comparison with Kano and Lagos, Jos had of known risk factors raises the question of a genetic pre-
lower rates of delayed care seeking, TSB >30 mg/dL, and disposition to ABE or exposure to unknown substances
lack of antenatal clinic attendance (P < 0.001). affecting bilirubin binding and emphasizes the need for more
detailed evaluation of those diagnosed with low TSB ABE.
Because of uncertainty about risk for low TSB ABE, access
Discussion to care, accurate rapid laboratory support, and guaranteed
power supply for phototherapy, some have promoted lower
This study confirms the high rate of ABE in Nigeria, with a TSB thresholds for initiating phototherapy in low-middle
incidence of nearly five cases per month in two of five income countries (LMICs) where ABE is prevalent [34].
U. M. Diala et al.

SHD (hematocrit ≤35% and TSB ≥20 mg/dL) was a unable to administer phototherapy or exchange transfusion,
major contributor to ABE. It is likely that the majority of but the contribution of intermediate care facility evaluation
cases with non-alloimmune SHD represent G6PDd hemo- to delay was not well documented. The most frequent
lytic crises. G6PDd is the most common cause of hyper- behavioral reason for delay, here and in other studies [2, 6,
bilirubinemia reported in Nigeria [35–37]. Between 5 and 14–17, 23], was a failure to recognize the severity of
26% of male infants have G6PDd in Nigeria, depending on jaundice or early signs of neurotoxicity (83%), again more
tribal genetic heritage [36]. The overall incidence of G6PDd common in out-of-hospital births [1, 17, 18, 23]. Failed
is estimated to be 16.9% (IQR 14–20) [37]. In Nigeria, trials of sun exposure, antibiotics or traditional medicines,
exposure to hemolytic triggers, e.g., decorative henna, and bad advice from health providers or family, economic
mentholated balms or naphthalene (“camphor”) is very and transportation issues have been cited in other reports
common [38–40]. Massey Street Children’s Hospital in [14, 19] but were minor contributors to delayed admission
Lagos had a disproportionately large number of newborns in this study population.
with non-alloimmune and presumably G6PDd SHD, but A common denominator to most of these harmful
exposure to hemolytic triggers was not consistently docu- behaviors was a lack of basic understanding about jaundice
mented. A World Health Organization study group on by both parents and healthcare providers [17–22, 43]. Low
G6PDd recommended newborn screening be conducted in maternal education (not assessed in this study) is associated
regions where there is a high incidence of G6PDd [41], but with higher risks for delayed care seeking and lack of
the cost of rapid screening is prohibitive for many indivi- knowledge about jaundice [17, 18, 22]. Unfortunately, even
duals (as in this study) and currently impractical to when mothers are equipped with this information, tradi-
administer for most home births. In the absence of universal tional practices and social pressures often obstruct trans-
screening in LMICs with high incidence of G6PDd, it lating knowledge into appropriate behavior [14, 18, 44].
would be prudent to consider all newborns to be at risk and While many have addressed the need to instruct providers
instruct all mothers to avoid exposing their infants to and parents about the risks of jaundice and need for early
hemolytic triggers [42]. assessment, there is little evidence that these interventions
Birth site per se should have little if any effect on serum change behaviors or, more importantly, prevent severe
bilirubin levels, but out-of-hospital births are associated hyperbilirubinemia and ABE.
with poor parental knowledge about jaundice and behaviors
that influence the response to jaundice [16–18]. In this Limitations
study, mothers giving birth at home had fewer antenatal
clinic visits, higher rates of delayed care seeking, and were The population served in this study may not be repre-
attended by TBAs, CHEWs or family members. Births sentative of the general population of states in which the
attended by TBAs and CHEWs were 2–4 times more likely centers are located. This was primarily an urban study and
to develop ABE than those born in clinics or hospitals and the incidence of ABE is likely to be higher in rural areas
attended by physicians. Birth attendants may be the only where quality of health care and percentage of home births
source for monitoring newborns and educating mothers is higher than we observed. An estimated 37% of births in
about jaundice in home births, and a recent study identified Nigeria occur in hospitals [45] whereas 66% of cases in
CHEWs as the primary source of jaundice information for this study were delivered in hospitals. National estimates
mothers [22], of unskilled birth attendants for Plateau, Kaduna, and
Unskilled birth attendants and home births were highly Kano States ranged from 69 to 87% [46] compared with
interdependent risk factors for ABE having similar AUC 4.7 to 34% in centers serving the same regions in this
results with ROC analysis, but in planning an intervention study. In contrast, unskilled providers delivered 74% of
strategy it will likely be easier to train birth attendants than newborns referred to Massey Street Children’s Hospital
to eliminate home births. while delivering only 17% of newborns in the entire Lagos
Irrespective of etiology, a delay in treating severe State [46].
hyperbilirubinemia was a critical factor contributing to the The considerable variation in ABE rates between parti-
high rate of ABE in this study. Only a small number of cipating centers helped to identify risk factors that were
patients were monitored and referred by health providers. unique to centers and common to all. However, we did not
The majority of admissions were self referrals. In Kano and measure or document several previously shown contributors
Lagos, centers with highest ABE rates, provider monitoring to ABE including G6PD activity, exposure to hemolytic
and referral was less than 3.5%, compared with 28–40% in triggers, maternal education, or prior awareness about
other centers. Hospital and clinic referrals (41% and 66%, jaundice and its risks. The study focused on pre-admission
respectively) were greater than other centers (17 to 29%), events rather than quality of treatment ABE. Other than
presumably because parents had first sought care at facilities monitoring and correcting irradiance during the study, no
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Acknowledgements This study was made possible in part through the of cerebral palsy in Nigeria: are doctors’ wrong beliefs and
generous support of the Saving Lives at Birth partners: the United practices part of the problem? Int J Med Biomed Res.
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lenges Canada, and the UK Government. It was prepared by the “Stop a major cause of death and disability in low and middle-income
Kernicterus in Nigeria” consortium and Bilimetrix, srl and does not countries? Arch Dis Child. 2014;99(12):1117–21.
necessarily reflect the views of the Saving Lives at Birth partners.” 15. Owa JA, Ogunlesi TA. Why we are still doing so many exchange
blood transfusion for neonatal jaundice in Nigeria. World J
Author contributions The study results from the concerted contribu- Pediatr. 2009;5(1):51–55.
tions of the entire “Stop Kernicterus in Nigeria” (SKIN) team who also 16. Ogunlesi TA, Ogunfowora OB. Predictors of acute bilirubin
reviewed and approved the manuscript. Trieste (ITA): C Greco, C encephalopathy among Nigerian term babies with moderate-
Tiribelli; Asaba (NGA): A Okolo, OU Chima; Lagos (NGA): Z to-severe hyperbilirubinaemia. J Trop Pediatr. 2011;57
Imam,; A Odunsi, S Olaifa; Jos(NGA): F Bode-Thomas, C Isichei, CS (2):80–86.
Yilgwan, Z Hassan, D Shwe, AO Ofakunrin, H Abdu, E Olagbaju, VC 17. Ogunlesi TA, Abdul AR. Maternal knowledge and care-seeking
Pam, JO Abba, SN Attah; Zaria(NGA): WN Ogala, LHassan, F behaviors for newborn jaundice in Sagamu, Southwest Nigeria.
Abdullahi, S Purdue; Kano(NGA): BW Jibir, IY Mohammed, HA Niger J Clin Pract. 2015;18(1):33–40.
Usman, M Abdusalam, SU Abdullahi, F Usman, A Kuliya-Gwarzo, FI 18. Ogunlesi T, Ogunlesi F. Family socio-demographic factors and
Tsiga-Ahmad, L Umar. maternal obstetric factors influencing appropriate health-care
seeking behaviours for newborn jaundice in Sagamu, Nigeria.
Matern Child Health J. 2012;16(3):677–84.
Compliance with ethical standards 19. Goodman OOK, Odugbemi BA, Femi-Adebayo TT, Odusanya
OO. Neonatal jaundice: knowledge, attitude and practices of
Conflict of interest The authors declare that they have no conflict of mothers in Mosan-Okunola community, Lagos, Nigeria. Niger
interest. Postgrad Med J. 2015;22(3):158–63.
20. Egube BA, Ofili AN, Isara AR, Onakewhor JU. Neonatal jaundice
and its management: knowledge, attitude, and practice among
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