Andrade et al. BMC Pediatrics (2020) 20:440 https://doi.org/10.1186/s12887-020-02334-z RESEARCH ARTICLE Open Access Pulse oximetry curves in healthy children living at moderate altitude: a cross- sectional study from the Ecuadorian Andes Vinicio Andrade1*, Felipe Andrade1, Pablo Riofrio1, Fúlvio B. Nedel2,3, Miguel Martin1,2,4 and Natalia Romero-Sandoval1,2 Abstract Background: In populations above 3,000 meters above sea level (m.a.s.l.) normal values of oxygen saturation (SpO2) above 90% have been reported. Few studies have been conducted in cities of moderate altitude (between 2,500 and 3,000 m a.s.l). We set out to describe the range of SpO2 values measured with a pulse oximeter in healthy children between 1 month and 12 years of age living in an Ecuadorian Andean city. Methods: A cross-sectional study was carried out in Quito, Ecuador, located at 2,810 m a.s.l. SpO2 measurement in healthy children of ages ranging from 1 month to 12 years of age residents in the city were recorded by pulse oximetry. Age and gender were recorded, and median and 2.5th and 5th percentile were drawn. Non parametric tests were used to compare differences in SpO2 values by age and gender. Results: 1,378 healthy children were included for the study, 719 (52.2%) males. The median SpO2 for the entire population was 94.5%. No differences were observed between SpO2 median values by age and gender. The 2.5th percentile for global SpO2 measurements was 90%, in children under 5 years of age was 91% and it was 90% in children older than 7. Conclusions: Our results provide SpO2 values for healthy children from 1 to 12 years old residents in Quito, a city of moderate altitude. The SpO2 percentile curve could contribute as a healthy range for the clinical evaluation of children residing at this altitude. Keywords: pulse oximetry: reference value, children, altitude Background and/or decreased oxygen saturation in arterial blood and Oxygen saturation (SpO2) is an indirect index of oxygen in this case, it should be called hypoxemia [4]. Hypox- supply-to-demand balance [1, 2]. Pulse oximetry pro- emia in children has been associated with increased vides information about patient’s oxygenation status and mortality and is a frequent complication in cases of is a reliable, simple, safe, accurate, and relative low cost pneumonia, bronchiolitis, asthma and other severe dis- method to monitor the patient as compared to expensive eases such as sepsis [5]. The recognition of hypoxemia and labor-intensive methods [3, 4]. Patient’s oxygenation among children with pneumonia contributes to diagno- status can show a reduced partial pressure of oxygen sis, is crucial in patient management, and helps in deter- mining prognosis [5–7]. The World Health Organization (WHO) recommends * Correspondence: vinanmay@gmail.com 1 School of Medicine, Universidad Internacional del Ecuador, Av. Simón an oxygen saturation threshold value of 90% measured Bolívar and Av. Jorge Fernández. Quito, Quito, Ecuador by pulse oximetry, as the cut-off point for oxygen Full list of author information is available at the end of the article © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Andrade et al. BMC Pediatrics (2020) 20:440 Page 2 of 7 administration in populations living at 2,500 m a.s.l. or was approved by the Universidad Internacional del less [6]. In clinical practice, the “normal” SpO2 at sea Ecuador Ethics Committee, registered code CEU-005-16 level has been estimated to be between 95% and 100%, and by the health committee at each center participating however, several authors consider that values of 95% and in the study. Information on the study was provided to 96% were abnormal [3]. In altitudes above 3,000 m a.s.l, the directive councils and medical teams at each where oxygen saturation values are lower than at sea institution. level, the 90% cut-off point could be less useful [8]. Fifteen students from fourth year of a school of medi- There are few studies about SpO2 values performed in cine were rigorously trained in anthropometric measure- cities between 2,000 and 3,000 m a.s.l [9–11]. In order to ments and pulse oximetry assessment by the contribute to the best comprehension about SpO2 values standardization method of the Central America and in healthy children living at moderate altitude, our study Panama Institute of Nutrition (INCAP) [14]. To manage was devised to describe the values range of SpO2 mea- measurement bias, the students’ measurements were sured with a pulse oximeter in healthy children between compared against a pediatrician’s reference pattern, es- 1 month and 12 years of age living at 2,810 m a.s.l. tablishing a maximum margin of error of 0.2 kg for weight and 0.5 cm for length and height [14]. Methods Subjects and methods Variable definition This cross-sectional study was conducted between Au- Weight and height were measured using high fidelity gust 2017 and June 2018. We invited 1,516 children resi- equipment (Health-o-Meter 498KL and 593KL, USA), dents in Quito, aged between 1 month and 12 years old, regulated and previously calibrated by the Ecuadorian who sought preventive medical attention at three pri- Institute of Normalization. Respiratory frequency was mary health-care centers (Lucha de los Pobres Health- obtained through observation in calm and alert children, care Center, Cotocollao Health-care Center and Clínica visually counting thoracic and abdominal movements Pichincha), three elementary schools (Escuela Francisco over one minute. Temperature was assessed with a flex- Salazar, Centro del Muchacho Trabajador Cotocollao ible digital thermometer (Omron MC-343F, Mexico), and Centro del Muchacho Trabajador La Marín) and placed in children’s armpit until a reading signal was ob- nine kindergarten municipal schools (Abdón Calderón, tained. Heart rate and SpO2 were evaluated using auto- Andalucía, Carapungo, Colibrí, Cotocollao, Empleados matically calibrated non-invasive pulse oximeters Municipales, Ipiales, La Carolina and Santa Clara) to (Huntleigh MP1R Smartsigns® MiniPulse Huntleigh participate. Non-probabilistic and convenience sampling Healthcare Ltd, Cardiff, United Kingdom). The pulse ox- were used because age and gender distribution at the imeter used measured functional oxygen saturation with schools and health-care centers was unknown. The cen- a precision range of ± 2%. Pulse oximetry was assessed ters are located at an altitude between 2,740 and 2, in calm and alert children. Wrap-around style and fold- 901 m a.s.l (average 2,810 m a.s.l). Ambient temperature over-style probes were used, depending on the subject’s throughout the study was, on average, 14.4 oC (11.5– age, and placed either on right hand’s index finger or the 20.8 oC) and humidity average was 72.2% (52–81%) as big toe for infants. Nail polish remover was provided for reported by Ecuador’s National Institute of Meteorology subjects who had nail polish present at the time of the and Hydrology[12]. test. The SpO2 measurements were considered adequate We included children who resided in the city at least 2 when a plethysmographic waveforms of perfusion months before the study, similar criteria used in other levelled-off on its high end and remained on the output study [13], and children younger than 2 months must screen for at least 2 minutes. Then, SpO2 measurements have been born and remain living in the city until they and pulse rate, were recorded every 10 seconds for a were examined. Exclusion criteria included a registered total of three measurements, and the average was used axillary temperature > 37.5 C° at the time of evaluation, to determine SpO2 for each study subject [6, 15–17]. history of respiratory symptoms in the two weeks prior to evaluation, any abnormal cardio-respiratory signs dur- Statistical Analysis ing physical examination, history of chronic cardio- Descriptive statistical tests were run for clinical mea- respiratory disease, history of neonatal respiratory dis- surements, and 2.5th percentile, 5th percentile, 25th per- ease, history of blood component transfusion in the six centile (Q1) and 75th percentile (Q3) for SpO2 months prior to evaluation, and the presence of malnu- distribution. The Kruskal-Wallis test was used to com- trition, defined as a Z-score less than − 2SD for either pare differences in SpO2 medians by age groups, Mann- height for age or weight for height [9, 10]. Whitney U test was used to compare medians between Children were enrolled in the study after written in- males and females. Statistical significance was accepted formed consent obtained from their parents. The study with p < 0.05. Smooth lines were designed for percentiles Andrade et al. BMC Pediatrics (2020) 20:440 Page 3 of 7 2.5th and 5th for SpO2 using the Spline method was between 89% and 90%, while in other age groups (smooth.spline function in R, with a 7 degree freedom the values recorded were between 90 and 91%. range). All data was registered in the digital survey plat- Figure 2 represents SpO2 percentile lines for male form Survey Monkey®, and analyses were performed population, value percentile 2.5th for SpO2 was between using SPSS®, version 24. Graphics were designed using R 89% and 90% for children younger than 1 year and of 8 version 4.3. and 9 years of age, respectively. Figure 3 represents the same data for females. Values 2.5th percentile for SpO2 Results were between 89% and 90% from 4 to 11 years of age. 1,516 children were invited to participate. A total of 1, No differences were observed by gender (Mann-Whitney 378 (90.9%) subjects were included for the study, of U test, z=-1,095 p = 0.273). which 719 (52.2%) were male. 138 children were ex- cluded of which 7 were for not being residents of Quito, Discussion 56 had fever, 141 presented any cardiorespiratory symp- The use of pulse oximetry is advised in order to increase toms, 31 presented stunting and 15 acute malnutrition. detection of hypoxemia, considering normal SpO2 range 13 had history of chronic cardiorespiratory disease, 3 values at higher altitudes [5, 8]. Some studies that re- had history of neonatal respiratory disease, and 1 had ported SpO2 measurements by average have showed blood transfusion prior. 55 (39.8%) had only one exclu- SpO2 value is close to 99% at sea level and appears to sion criteria and 8 (5.8%) had 4. Measurements charac- decrease to 97% after 1500 to 1600 m a.s.l [15, 17, 18]. teristics of the included group are listed in Table 1. Furthermore, at 3000 m a.s.l, mean SpO2 values of 89.6% [19] or even 85.7% have been reported [20]. The overall SpO2 lowest and highest values were 87% Lozano et al. at Bogotá-Colombia (2600 m a.s.l) have re- and 99%. Median, 2.5th, 5th, 25th (Q1) and 75th per- ported mean SpO2 value of 93.3% (SD 2.05%) [10] and centile (Q3) for SpO2 by age are listed in Table 2. Nicholas et al. at Colorado-USA (2800 m a.s.l) of 91.7% (SD 2.1%) [9]. Because SpO2 levels are not normally dis- SpO2 at 12 years of age was the lowest median value tributed, it seems appropriate to report the data in me- (94%), and the highest median value was observed in dian values and percentile values [8]. We present a curve children aged 1 year (95%); no significant differences in with the medians and 5th and 2.5th percentiles of SpO2 SpO2 median values were found between age (Kruskal- of children from 1 month to 12 years permanent resi- Wallis Chi square test = 7.94, df = 11, p = 0.72). dents in the city of Quito, at 2810 m a.s.l. We did not Figure 1 shows the smooth percentile lines for SpO2 find significant differences by children age or sex. corresponding to percentiles 5th and 2.5th in all partici- The median for global SpO2 measurements was pants by age. It is noteworthy that in children between 94.67%, 5th percentile was 91.67%, and 2.5th percentile the ages of 7 and 9 the SpO2 value for percentile 2.5th was 90.67%. Rojas-Camayo et al. in children aged 1 to 5 Table 1 Clinical measurements characteristics by age group (mean and standard deviation) Age (years) n (percentage of total) HR beats/min RR breaths/min BMI Kg/m2 Height m Temp oC mean (SD) mean (SD) mean (SD) mean (SD) mean (SD) <1 167 (12.1) 132.8(14.3) 43.6 (9.2) 16.6(1.8) 0.64(0.1) 36.8(0.2) 1 58 (4.2) 125.4(12.0) 33.8(5.4) 16.4(1.4) 0.78(0.1) 36.7(0.4) 2 149 (10.8) 113.4(10.9) 30.1(4.4) 16.27 (1.4) 0.87(0.0) 36.6(0.4) 3 154 (11.2) 105.9(11.2) 27.1(3.6) 16.0(1.3) 0.95(0.1) 36.6(0.4) 4 155 (11.2) 100.6 (11.2) 26.0 (3.3) 16.0(1.4) 1.00(0.0) 36.6(0.4) 5 111 (8.1) 98.4(11.9) 25.9 (3.1) 16.0 (1.3) 1.06(0.1) 36.6(0.4) 6 74 (5.4) 88.8(12.6) 24.5(3.8) 16.1(2.4) 1.13(0.1) 36.7(0.4) 7 101 (7.3) 91.7 (12.4) 26.1(3.5) 16.3(1.9) 1.19(0.6) 36.6(0.4) 8 93. (6.7) 88.0 (11.1) 25.9 (3.9) 17.0 (2.3) 1.24(0.1) 36.7(0.4) 9 96 (7.0) 87.9(12.6) 25.2(4.3) 17.0 (1.9) 1.28(0.6) 36.6(0.4) 10 85 (6.2) 84.0(11.4) 24.8(3.9) 17.5 (2.1) 1.33(0.1) 36.5(0.4) 11 100 (7.3) 82.2(11.1) 24.1(3.9) 18.1(2.4) 1.38(0.1) 36.6(0.4) 12 35 (2.5) 83.0 (11.3) 24.0 (2.7) 18.1(1.9) 1.41(0.1) 36.5(0.4) Heart Rate (HR) defined as beats per minute. Respiratory Rate (RR) defined as breaths per minute. Body Mass Index (BMI). Height measured in meters (m) and Body temperature measured in Celsius degrees (°C). Andrade et al. BMC Pediatrics (2020) 20:440 Page 4 of 7 Table 2 Distribution of oxygen saturation measured by pulse oximetry by age Age (years) Median 2.5th Percentile 5th Percentile 25th Percentile (Q1) 75th Percentile (Q3) <1 95.1 90.0 91.3 93.7 96.7 1 95.3 91.9 92.7 94.3 96.0 2 95.0 90.7 91.8 93.7 96.0 3 95.0 91.8 92.3 94.0 96.0 4 95.0 90.6 91.6 94.0 95.7 5 94.3 91.3 91.7 93.3 95.3 6 94.3 90.4 91.2 93.3 95.7 7 94.3 90.2 91.6 95.3 95.7 8 94.3 90.2 91.6 93.3 95.3 9 94.3 89.2 91.6 93.0 95.3 10 94.3 90.7 91.3 93.3 95.3 11 94.0 91.0 96.7 93.0 95.0 12 93.8 90.7 91.8 92.8 94.7 Global 94.7 90.7 91.7 93.4 96.7 years, report at 2880 m a.s.l, SpO2 median value of 95%, the accuracy of pulse oximeters (+ -2%). With this 2.5th percentile was 91% [21]. In a recent study, Tüshaus model, the median at 2800 m a.s.l was 93% with lower et al. obtained an altitude-adaptive SpO2 computer healthy range of 88%, and abnormal SpO2 threshold of model and proposed a model derived altitude-adaptive 86%. To evaluate the model, the authors compared it abnormal SpO2 threshold for an abnormal range that with an empirical dataset of 297 children residing be- could indicate hypoxemia, in healthy children living per- tween 2000 and 3900 m a.s.l. In that empirical study, manently at altitudes up to 4000 m a.s.l [11]. They used they report that at an altitude of 2800 m a.s.l median the physiological model of the oxygen cascade and in- SpO2 was 95.2% and 2.5th percentile was 90%[11]. Our corporated the technical tolerances that accounted for median and 2.5th percentile values presented similar Fig. 1 SpO2 percentile values by age. Children residents in Quito, august 2017-june 2018 Andrade et al. BMC Pediatrics (2020) 20:440 Page 5 of 7 Fig. 2 SpO2 percentile values for age in boys residents in Quito, august 2017-june 2018 Fig. 3 SpO2 percentile values for age in girls residents in Quito, august 2017-june 2018 Andrade et al. BMC Pediatrics (2020) 20:440 Page 6 of 7 results to those of Rojas-Camayo and the empirical study obtained cannot apply to patients who have not adapted of Tüshaus et al. According to the physiological model to altitude. (2) All children in the sample had their med- of Tüshaus et al., the median value is similar, but the ical records and physical examination taken but did not 2.5th percentile is lower. It is possible that this difference undergo laboratory testing for parameters such as serum is due to the fact that the altitude-adaptive model is hemoglobin, arterial blood gas testing or chest X-rays to physiological and takes into account the pulse oximeters discard other pathologies not found on clinical evalu- accuracy. ation. (3) Although we carry out a standardization of Pulse oximetry is a non-invasive and relative low-cost personnel in the use of the pulse oximeter, we cannot assessment method able to reduce child mortality by ac- totally exclude possibilities of error in the measurement curately diagnosing hypoxemia, increasing the possibilities of SpO2 such as incorrect positioning of the probe or in- of early and effective treatment [21]. Unreal SpO2 values sufficient perfusion. (4) In this study we did not set out to could increase hospital admissions and hospital stays with compare the SpO2 results between the group that met the subsequent iatrogenic risks and misuse of resources [21, inclusion criteria with the excluded group; However, this 22]. Without pulse oximetry, the management of pediatric comparison could provide additional information. patients depends on precise identification of the clinical signs of hypoxemia, which are not always easy to assess in Conclusions all patients. Clinical signs alone are unreliable for the de- Our results provide SpO2 values for healthy resident tection of hypoxaemia [23]. children from 1 to 12 years old at 2810 m. a.s.l., which Pulse oximetry identifies between 20 and 30% more could be considered as healthy ranges. SpO2 percentile cases than clinical signs alone [21, 22, 24, 25]. However, curve could contribute as a reference range for the clin- the determination of a threshold to identify hypoxemia ical evaluation of resident’s children at this altitude. is difficult, especially in high altitude populations [26]. Some studies have previously used average SpO2 values Abbreviations SpO2: Oxygen Saturation; WHO: World Health Organization; m a.s.l: Meters -2 SD to define hypoxemia, however others have used above sea level; UIDE: Universidad Internacional del Ecuador the 2.5th percentile measurement as a cut-off point to decide to use oxygen [8]. Subhi et al., developed a statis- Acknowledgements The authors express their gratitude to children, their parents and teachers for tical model of SpO2 distribution from sea level to their participation in the study. We thank also students of School of 4000 m a.s.l. using meta regression based on 14 observa- Medicine for their support in the fieldwork. tional studies of healthy children. At an altitude of Authors’ contributions 2500 m a.s.l the 2.5th percentile was 90% and at 2800 m VA and NR conceptualized and designed the study, drafted the initial a.s.l was 88%. It suggests that for altitudes greater than manuscript, and reviewed and revised the manuscript. PB and FA designed 2500 m a.s.l the SpO2 threshold for identifying children the data collection instruments and collected data. MM and FN carried out the initial analyses and reviewed and revised the manuscript. All authors requiring oxygen is 85% although it is not clearly defined approved the final manuscript as submitted and agree to be accountable for how the threshold was chosen [8]. The threshold ob- all aspects of the work. tained with the Tüshaus altitude-adaptive model at 2800 m.a.s.l was 86% [11]. It is possible, that our results Funding All phases, design of the study and collection, analysis, and interpretation of are related to “normality” in “children at community data and in writing the manuscript were supported by Universidad settings without respiratory symptoms and not fever Internacional del Ecuador, grant number EDM-INV-11-17. Dr. Nedel, who par- living at moderate altitude”, however, the 2.5th per- ticipated in analysis, interpretation of data and in writing the manuscript was supported by Universidad Federal de Santa Catarina. Dr. Martin who partici- centile values could be conservative to be considered pated in design, analysis, interpretation of data and in writing the manuscript as a threshold to define hypoxemia or the need to ad- was supported by Universidad Autonoma de Barcelona. minister supplemental oxygen. It is very important to Availability of data and materials consider the accuracy range of the pulse oximeter Non-identified individual participant data (including data dictionaries) will be used (+-2%) [11]. made available, in addition to study protocols, the statistical analysis plan, Physicians should consider the patient’s clinical condi- and the informed consent form. The data that support the findings of this study are available in DSpace in the following identifier https://repositorio. tion to make the decision to use oxygen therapy, espe- uide.edu.ec/handle/37000/4228. The data will be made available upon cially in places where we have limited availability of publication to researchers who provide a methodologically sound proposal resources. It would be important to evaluate SpO2 in for use in achieving the goals of the approved proposal. Proposals should be submitted to vinanmay@gmail.com. children with low respiratory disease at moderate alti- tude to propose cut-off points for supplemental oxygen Ethics approval and consent to participate administration. Subjects were enrolled in the study after written informed consent obtained There are some limitations to the study. (1) Measure- from their parents. The study was approved by the Universidad Internacional del Ecuador Ethics Committee registered code CEU-005-16, and by the ments were carried out in children between 1 month health committee at each center participating in the study. 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