Blackwell Publishing AsiaMelbourne, AustraliaJPCJournal of Paediatrics and Child Health1034-4810 2007 The Authors; Journal compilation 2007 Paediatrics

s and Child Health Division (Royal Australasian College of Physicians)? 2006434297302Original ArticleBilicheck and severe jaundiceN-Y Boo and S Ishak

doi:10.1111/j.1440-1754.2007.01062.x

ORIGINAL ARTICLE

Prediction of severe hyperbilirubinaemia using the Bilicheck transcutaneous bilirubinometer

Nem-Yun Boo and Shareena Ishak
Department of Paediatrics, Faculty of Medicine, Universiti Kebangsaan Malaysia, Jalan Yaacob Latif, 56000 Kuala Lumpur, Malaysia.

Objectives: To determine the sensitivity and specicity of different levels of bilirubin measured by the transcutaneous bilirubinometer Bilicheck on forehead and sternum for predicting severe hyperbilirubinaemia of total serum bilirubin (TSB) 300 mol/L in Malay, Chinese and Indian infants. Design: A prospective observational study. Setting: A tertiary care University hospital. Methods: A total of 345 healthy jaundiced term infants were recruited prior to commencement of phototherapy or exchange transfusion. Transcutaneous bilirubin (TcB) level was measured with the Bilicheck from infants foreheads (TcBh) and sternums (TcBs) within 30 min of serum bilirubin measurement by the diazo method in the hospital laboratory. Results: The median serum TSB level of these infants was 233.0 mol/L (range: 108.0589.0). Ninety-ve (27.5%) infants had TSB 300 mol/ L. There was good correlation between log10TSB and TcB measured from the forehead (r = 0.80, P < 0.0001) and the sternum (r = 0.86, P < 0.0001). At TcBh cut-off of 250 mol/L, the Bilicheck detected TSB 300 mol/L with a sensitivity of 100% and a specicity of 39.2%, the area under the receiver operative characteristic curve being 0.89 (95% condence interval 0.85, 0.92). At TcBs cut-off of 200 mol/L, the Bilicheck detected TSB 300 mol/L with a sensitivity of 100% and a specicity of 33.6%, the area under receiver operative characteristic curve being 0.93 (95% condence interval 0.90, 0.96). Conclusion: The Bilicheck is not a substitute for measuring serum bilirubin. However, using predetermined TcB cut-off values with reasonable sensitivity and specicity, it is a useful screening tool to identify infants with TSB 300 mol/L requiring blood sampling, hospital admission and treatment. Key words: newborn; severe hyperbilirubinaemia; transcutaneous bilirubinometry.

The danger of severe neonatal hyperbilirubinaemia is irreversible neurotoxocity (kernicterus). Early detection of rising hyperbilirubinaemia is important for timely management to prevent brain damage. The most common initial step used to diagnose hyperbilirubinaemia is visual evaluation of the skin, sclera and mucous membranes of infants. However, quantication of the severity of hyperbilirubinaemia in newborns based on visual

Key Points 1 At high total serum bilriubin (TSB) level, there is an exponential relationship between TSB and transcutaneous bilirubin (TcB) measurement. 2 High TSB 300 mol/L can be predicted with 100% sensitivity at certain TcB cut-off levels measured at the forehead and sternum of infants. 3 The Bilicheck is not a substitute for measuring serum bilirubin.
Correspondence: Professor Nem-Yun Boo, Clinical School, International Medical University, Jalan Rasah, 70300 Seremban, Negeri Sembilan, Malaysia. Fax: +606 767 7709; email: nemyun_boo@imu.edu.my Accepted for publication 14 December 2006.

estimation is subjective and inaccurate, often confounded by skin pigmentation. The conventional methods of measuring total serum bilirubin (TSB) require blood sampling, which not only causes pain to infants but also causes parental stress. Moreover, repeated blood sampling is associated with risk of infection and scar formation. Depending on the location of laboratory services, there may be delay before TSB results are available for commencement of treatment. Over the last two decades, transcutaneous bilirubinometry has been developed as a non-invasive, safe, painless and convenient method of estimation of TSB and it provides instant results. The principle of older models of transcutaneous bilirubinometer was based on measurement of reected light from the skin using two wavelengths (460 and 520 nm) and provided a numerical index based on spectral reectance. The accuracy of estimation of TSB, however, was limited by the confounding effect of skin pigmentation.1,2 In recent years, a newer generation of transcutaneous bilirubinometers has been marketed. They differ from earlier models as they have a micro spectrophotometer that determines the optical densities of bilirubin, haemoglobin and melanin in the subcutaneous layer of the infants skin. Mathematical isolation of optical densities of interfering factors allows measurement
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Bilicheck and severe jaundice

N-Y Boo and S Ishak

of the optical density created by the bilirubin in capillary beds and subcutaneous tissue.1 One of these newer transcutaneous devices is the Bilicheck (SpectRx Inc., Norcross, GA, USA), which measures skin bilirubin using reection rate of multiwavelength spectra (380760 nm) and provides a transcutaneous bilirubin (TcB) measurement. A number of large series studies have reported on the significant correlation between the Bilicheck TcB readings and TSB in predominantly Caucasian1,35 and Japanese neonates.6 However, not many non-Japanese Asian neonates were recruited in these studies. Furthermore, most studies did not recruit large enough number of infants with severe hyperbilirubinaemia of TSB 300 mol/L. Studies on primarily Hispanic7 and Indian infants8 who were more pigmented than Caucasians showed that despite the signicant correlation between TSB values and the Bilicheck TcB, TcB determinations underestimated TSB, especially in infants with relatively high TSB values. In addition, TcB measured from the forehead showed better correlation with TSB than when measure from the chest in predominantly fair skinned Caucasian4 and Japanese6 infants. In multiracial Malaysia, the prevalence of severe neonatal hyperbilirubinaemia requiring phototherapy and exchange transfusion was high (32.4 per 1000 live births), with a prevalence of kernicterus of 0.9%.9 Our research question was whether transcutaeous bilirubimeter Bilicheck could predict accurately infants with severe hyperbilirubinaemia of TSB 300 mol/L. The objectives of the present study were to determine the sensitivity and specicity of different levels of bilirubin measured by the transcutaneous bilirubinometer Bilicheck on the forehead and sternum for predicting severe hyperbilirubinaemia of TSB > 300 mol/L in Malay, Chinese and Indian infants.

quality control and participated in external quality assurance scheme (Royal College of Pathologists of Australasia Quality Assurance Program). At the time of the study, the measurements of serum bilirubin were within acceptable limits of variation.

Transcutaneous bilirubin estimation

TcB levels of infants were measured using the Bilicheck device. It consisted of a light source, a micro spectrophotometer, a breoptic probe and a microprocessor control circuit with rmware for analysis and interpretation of bilirubin housed in a handheld assembly.3 Just prior to each measurement, the device was calibrated using a disposable standard reference placed in direct contact with its probe. The probe was then placed on the infants skin using light pressure. The light source of the device was triggered for 5 spectral collections, which were averaged to one TcB measurement. The TcB of each infant was measured from its forehead (TcBh) and at the midpoint of its sternum (TcBs). During TcBh measurement, the probe of Bilicheck was placed such that it was away from an infants hairline and at a site free of bruises, haematoma and local nevus.

Calculation of sample size

In order to recruit sufcient number of infants with severe hyperbilirubinaemia based on a reported prevalence of hyperbilirubinaemia of 75%11 with an absolute precision of 5% and 95% condence, a sample size of at least 288 jaundiced infants was required.12

Statistical analysis
The statistical package SPSS (version 10.1, Chicago, IL, USA) was used for analysis of data. Demographic data among the three ethnic groups were compared. Analysis of variance (ANOVA) was used for analysis of continuous variables with normal distribution. Bonferroni test was used for post hoc analysis. KruskallWallis test was used for analysis of continuous variables with skewed distribution. Chi-squared test was used for analysis of categorical variables. The TcB values of infants were plotted against their TSB except those without numeric TcB readings, and their coefcient of correlation calculated. In the presence of an exponential relationship between these two variables, logarithmic transformation was carried out before calculation of coefcient of correlation. In order to determine whether the difference between TSB and TcB measurements was related to the magnitude of the measurement, the difference between TSB and TcB was plotted against the average of TSB and TcB measurements.13 As the highest displayed value of TcB obtained during the study was 342 mol/L, infants whose Bilicheck reading displayed very high values were assigned a TcB values of 300 mol/L during calculation of sensitivity and specicity in predicting TSB at different cut-off values. Receiver operative characteristic (ROC) curves were constructed to determine the TcB value at which the sensitivity reaches 100% in predicting TSB levels of 250 mol/L, 280 mol/L and 300 mol/L.
Journal of Paediatrics and Child Health 43 (2007) 297302 2007 Paediatrics and Child Health Division (Royal Australasian College of Physicians)

Methods
This was an observational study carried out over a 25-month period (between January 2003 and January 2005) in the postnatal wards and neonatal intensive care unit of the Hospital Universiti Kebangsaan Malaysia. The inclusion criteria were healthy Malaysian term (37 weeks of gestation) neonates with hyperbilirubinaemia. The exclusion criteria were infants who had received phototherapy or exchange transfusion prior to recruitment into the study, multiple congenital abnormalities or severely ill infants, foreigners, or those with conjugated hyperbilirubinaemia of >34 mol/L. Parental consent was obtained before recruitment. The study protocol was approved by the Institution Research and Ethics Committee.

Measurement of serum bilirubin

Venous blood (0.5 mL) was collected from each jaundiced infants for measurement of serum bilirubin within 30 min of measurement of TcB. To prevent photo-conversion of bilirubin in the blood samples, specimen bottles were covered with thick paper labels. Blood samples were assayed, by the diazo method using the Cobas Integra system (Roche Diagnostics, Basel, Switzerland),10 in the hospital routine service laboratory. Technicians who measured the TSB had no knowledge of the TcB readings of the infants. This laboratory carried out internal
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Bilicheck and severe jaundice

Table 1 Basic characteristics and clinical variables of term infants with hyperbilirubinaemia Basic characteristic and clinical variables Mean birthweight, g (SD) Gestational age, weeks Median (50% CI) Male sex (%) Ethnic groups (%) Malays Chinese Indians Age when serum bilirubin was measured, hours Median (50% CI) Range Total serum bilirubin, mol/L Median (50% CI) Range Indirect serum bilirubin, mol/L Median (50% CI) Range CI, condence interval; SD, standard deviation. n = 345 3056 (487)

Forehead
500 400

300

38 (37, 39) 207 (60) 220 (63.8) 106 (30.7) 19 (5.5) 70.0 (46, 103.5) 9.0388 233 (184, 307) 108589 220 (173, 295) 98572

TSB, mol/L

200

100 100 150 200 250 300 350 400

TcBh, mol/L

Sternum
500 400

300

Results
During the study period, 345 healthy full-term infants were recruited. Table 1 shows the basic and clinical variables of these infants. Ninety-ve (27.5%) of them had severe hyperbilirubinaemia (TSB 300 mol/L). There were no signicant difference in the mean birthweight, gender distribution, methods of delivery, and proportion of infants who were small for gestational age among the three ethnic groups (P > 0.05). Although they were all term infants, the median gestational age of Chinese infants (39.0 weeks, interquartile range (IQR) = 2.0) were signicantly greater than those of Malays (38.0 weeks, IQR = 2.0) and Indians (38.0 weeks, IQR = 3.0) (P = 0.02). There was no signicant difference in the median age when bilirubin levels were measured among the three ethnic groups (P = 0.3). Neither was there any signicant difference in the proportion of infants with severe hyperbilirubinaemia among the three ethnic groups (Malays: 27.2%, Chinese: 26.4%, Indians: 31.6%; P = 0.9). When measured from the infants foreheads, the Bilicheck displayed a numeric value of TcBh in 334 (96.8%) infants, with a mean TcBh of 232.1 mol/L (SD = 50.8; range: 125.0338.0). In the remaining 11 (3.2%) infants, the Bilicheck displayed a message very high values only; 10 of these infants had TSB levels ranging from 318 to 589 mol/L, while one had TSB = 268 mol/L at 42 h of age. When plotted against TcBh values, the TSB showed an exponential relationship with TcBh, as TSB values increased steeply at higher levels of TcBh. Figures 1 and 2 show that there is good correlation between log10TSB and TcBh in all infants (r = 0.80, P < 0.0001) and those of different ethnic groups, respectively. When measured from the infants sternums, the Bilicheck displayed a numeric value in 323 (93.6%) infants with a mean TcBs of 240.9 mol/L (SD = 53.3; range: 126342 mol/L). In
Journal of Paediatrics and Child Health 43 (2007) 297302 2007 Paediatrics and Child Health Division (Royal Australasian College of Physicians)

TSB, mol/L

200

100 100 150 200 250 300 350 400

TcBs, mol/L

Fig. 1 Relationship between transcutaneous bilirubin measured on forehead (TcBh), sternum (TcBs) and total serum bilirubin (TSB) of healthy Malaysian term infants (n = 334). The lines represent the regression prediction line of individual observations and their 95% condence intervals. On the forehead: coefcient of correlation r = 0.80, P < 0.0001; linear regression equation is log10TSB = 1.9 + 0.002TcBh, r2 = 0.6. On the sternum: coefcient of correlation r = 0.86, P < 0.0001; linear regression equation is log10TSB = 1.8 + 0.002TcBs, r2 = 0.7.

the remaining 22 infants, whose TSB were 300 mol/L, the Bilicheck displayed a message of very high values only. When plotted against TcBs values, the TSB showed an exponential relationship with TcBs, as TSB values increased steeply at higher levels of TcBs. Similarly, there was good correlation between log10TSB and TcBs levels (r = 0.86, P < 0.0001) in all the infants (Fig. 1), and those of different ethnic groups (Fig. 2). Measurement of TSB and TcB was carried out at a later age (>80 h of age) in a higher proportion of infants with severe hyperbilirubinaemia of TSB 300 mol/L (n = 75 or 78.9%) than those without severe hyperbilirubinaemia (n = 57 or 22.8%). The correlation between TSB and TcB of infants measured at 80 h of age (r = 0.85, P < 0.0001) was better than those measured after 80 h of age (r = 0.71, P < 0.0001).
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Forehead
Malay
500 400

Sternum
Malay
500 400

TSB, mol/L

TSB, mol/L

300

300

200

200

100 100 150 200 250 300 350 400

100 100 150 200 250 300 350 400

TcBh, mol/L

TcBs, mol/L

Chinese
500 400 300 300 400

Chinese

TSB, mol/L

TSB, mol/L

200

200

100 100 150 200 250 300 350 400

100 100 150 200 250 300 350 400

TcBh, mol/L

TcBs, mol/L

Indian
500 400
500 400

Indian

300

300

TSB, mol/L

TSB, mol/L

200

200

100 100 150 200 250 300 350 400

100 100 150 200 250 300 350 400

TcBh, mol/L

TcBs, mol/L

Fig. 2 Relationship between transcutaneous bilirubin measured on foreheads (TcBh), sternums (TcBs) and total serum bilirubin (TSB) of healthy Malaysian term infants of Malay (n = 214), Chinese (n = 102) and Indian (n = 18) ethnic groups. The lines on each scatter graph represent the regression prediction line of individual observations and their 95% condence intervals. On the forehead: Malay infants: coefcient of correlation r = 0.79, P < 0.0001; Chinese infants: r = 0.84, P < 0.0001; Indian infants: r = 0.83, P < 0.0001. On the sternum: Malay infants: r = 0.86, P < 0.0001; Chinese infants: r = 0.86, P < 0.0001; Indian infants: r = 0.94, P < 0.0001.

300

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N-Y Boo and S Ishak

Bilicheck and severe jaundice

Forehead
200

TSB 300 mol/L

1.00 .90

100

.80 .70

TSB-TcBh, mol/L

Sensitivity

.60 .50 .40 .30 .20

-100

-200 100 200 300 400

.10 0.00 0.00 .20 .40 .60 .80 1.00

Sternum Forehead

Average of TSB and TcBh, mol/L

Sternum
200

1 - Specificity

TSB 280 mol/L

1.00 .90

100

TSB-TcBs, mol/L

.80 .70

Sensitivity

.60 .50 .40 .30 .20

-100

-200 100 200 300 400

.10 0.00

Sternum Forehead .20 .40 .60 .80 1.00

Average of TSB and TcBs, mol/L

0.00

Fig. 3 Difference between total serum bilirubin (TSB) and transcutaneous bilirubin measurement on the forehead (TcBh) and sternum (TcBs) against the average of TSB and TcB. The lines indicate lines of agreement where TSB TcB = 0 mol/L.

1 - Specificity

TSB 250 mol/L

1.00 .90

Figure 3 shows that the difference between TSB and TcB widened more markedly from the line of agreement at average level of TSB and TcB above 250 mol/L, especially when TcB was measured from infants forehead. Figure 4 shows the ROC curves for TcBh and TcBs cut-off values when TSB was 250 mol/L, 280 mol/L and 300 mol/L, respectively. The areas under the curves for different TSB levels are slightly, but consistently, bigger for TcBs than for TcBh. At TcBh cut-off of 250 mol/L, it detected
Fig. 4 ROC curves for transcutaneous bilirubin cut-off values measured on foreheads and sternum when total serum bilirubin (TSB) of 300 mol/ L, 280 mol/L and 250 mol/L, respectively, are the outcomes of interest in healthy Malaysian term infants. The areas under the curves when: TSB 300 mmol/L: forehead = 0.89 (95% CI: 0.85, 0.92), sternum = 0.93 (95% CI: 0.90, 0.96); TSB 280 mol/L: forehead = 0.87 (95% CI: 0.83, 0.91), sternum = 0.94 (95% CI: 0.91, 0.97); TSB 250 mol/L: forehead = 0.89 (95% CI: 0.85, 0.92), sternum = 0.93 (95% CI: 0.90, 0.96).

.80 .70

Sensitivity

.60 .50 .40 .30 .20 .10 0.00 0.00 .20 .40 .60 .80 1.00 Sternum Forehead

1 - Specificity

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TSB 300 mol/L with a sensitivity of 100% and a specicity of 39.2%. At TcBh cut-off of 260 mol/L, it detected TSB 300 mol/L, with a sensitivity of 75.8% and a specicity of 84.8%. At TcBs cut-off of 200 mol/L, it detected TSB 300 mol/L with a sensitivity of 100% and a specicity of 33.6%. At TcBs cut-off of 280 mol/L, it detected TSB 300 mol/L with a sensitivity of 92.6% and a specicity of 84.0%.

In conclusion, the Bilicheck is not a substitute for measuring serum bilirubin in infants with hyperbilirubinaemia. However, using either a reference chart and/or predetermined TcB cut-off value with acceptable sensitivity and specicity from study in the local population, it is a useful screening tool to identify infants with severe hyperbilirubinaemia of TSB 300 mol/L requiring hospital admission, blood sampling and intensive phototherapy.

Discussion
Unlike previous reports, a much larger number of infants (n = 95) with severe hyperbilirubinaemia (TSB 300 mol/L) were recruited in the present study. This is the rst study which shows that the Bilicheck machine is not able to provide a reading of TcBh in 10.5% (10/95) and of TcBs in 23.2% (22/95) of infants with severe hyperbilirubinaemia. However, the device did display a written message of very high values in these infants. Despite this absence of a numerical reading, the Bilicheck device was able to predict severe hyperbilirubinaemia with 100% sensitivity at TcBh cut-off of 250 mol/L and TcBs cut-off of 200 mol/L, making it a very useful tool for detecting severe hyperbilirubinaemia in outpatient or home settings. Unlike those of other studies which showed good correlation between TcB readings and TSB,18 our results showed that there was signicantly good correlation between TcB readings and log10TSB from mild to severe hyperbilirubinaemia. Contrary to what was reported in predominantly Caucasian4 and Japanese infants,6 our results concurred with those of Poland et al.14 which reported better correlation of TcBs with TSB than TcBh with TSB. One possible explanation for this phenomenon in the Malaysian infants could be due to the greater hairiness of their foreheads, which possibly interfered with TcBh readings, than their sternum. Similar to the ndings of other studies,7,8 the predictive intervals of TcB measured from both the foreheads and sternums of infants were wide. In this study, a much larger proportion of infants with severe hyperbilirubinaemia had TSB and TcB assessed after 80 h of age than those with milder hyperbilirubinaemia. As newborn infants skin become thicker with age after birth, this could probably affect the TcB readings and contributed to the exponential relationship between TSB and TcB at higher values in this study. For clinicians, the most important feature of a good bedside bilirubinometer is its ability to detect severe hyperbilirubinaemia with 100% sensitivity at a reasonable level of specicity. Missing a case of severe hyperbilirubinaemia with resultant kernicterus is totally unacceptable, yet over-diagnosing infants with severe hyperbilirubinaemia results in unnecessary admission and parental stress. The present study shows that although TcB values measured with the Bilicheck correlates signicantly with log10TSB, its wide predictive interval precludes it as a reliable tool to predict the exact levels of TSB of infants. One way to minimise this problem of under- and over-diagnosis of severe hyperbilirubninaemia is to use reference charts like Figures 1 and 2 based on local population to guide clinicians in predicting the possible levels of the TSB of jaundiced infants in the clinics, assisted by TcB cut-off values with reasonable sensitivity and specicity.
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Acknowledgement
This study was supported by a research grant (no. FF-072-2002) from the Faculty of Medicine, Universiti Kebangsaan Malaysia.

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Journal of Paediatrics and Child Health 43 (2007) 297302 2007 Paediatrics and Child Health Division (Royal Australasian College of Physicians)