Assessment of Hypoxemia among Young Adults with Sickle Cell Anaemia in Steady State: A cross‑sectional study

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Objectives: Hypoxia is a known feature of sickle cell anaemia (SCA) which results from chronic anaemia and recurrent vaso-occlusive crisis which can cause tissue ischaemia that leads to an end organ damage. The hallmark of SCA is chronic anaemia and recurrent vaso-occlusive crisis. The aim of this study is to compare the oxygen saturation of sickle cell anaemic individuals with the normal haemoglobin type (Hb AA) control and also to determine the prevalence of hypoxemia among SCA. Results Two-hundred and twenty-two (136 Hb SS and 86 Hb AA) participated in the study. The mean ± SD of age (years), oxygen saturation (%) and pulse rate (bpm) of participants with sickle cell anaemia and Hb AA control were 21.85 ± 3.04 and 22.14 ± 3.18 (t = 0.701, p = 0.436), 95.21 ± 3.02 and 98.07 ± 0.81 (t=-8.598, p < 0.0001) and 77.10 ± 9.28 and 73.16 ± 8.52 (t = 3.173, p = 0.002) respectively. The prevalence of hypoxemia among SCA participants was 47.1%. Prevalence of hypoxemia in males with SCA was 60.9% while 39.1% of the females had hypoxemia.
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Assessment of Hypoxemia among Young Adults with Sickle Cell Anaemia in Steady State: A cross‑sectional study | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Short Report Assessment of Hypoxemia among Young Adults with Sickle Cell Anaemia in Steady State: A cross‑sectional study Muritala A. Asafa, Ibrahim O. Ahmed, Michael S. Afolabi, Rahman A. Bolarinwa, and 1 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-3135169/v1 This work is licensed under a CC BY 4.0 License Status: Published Journal Publication published 08 Apr, 2024 Read the published version in BMC Research Notes → Version 1 posted 10 You are reading this latest preprint version Abstract Objectives Hypoxia is a known feature of sickle cell anaemia (SCA) which results from chronic anaemia and recurrent vaso-occlusive crisis which can cause tissue ischaemia that leads to an end organ damage. The hallmark of SCA is chronic anaemia and recurrent vaso-occlusive crisis. The aim of this study is to compare the oxygen saturation of sickle cell anaemic individuals with the normal haemoglobin type (Hb AA) control and also to determine the prevalence of hypoxemia among SCA. Results Two-hundred and twenty-two (136 Hb SS and 86 Hb AA) participated in the study. The mean ± SD of age (years), oxygen saturation (%) and pulse rate (bpm) of participants with sickle cell anaemia and Hb AA control were 21.85 ± 3.04 and 22.14 ± 3.18 (t = 0.701, p = 0.436), 95.21 ± 3.02 and 98.07 ± 0.81 (t=-8.598, p < 0.0001) and 77.10 ± 9.28 and 73.16 ± 8.52 (t = 3.173, p = 0.002) respectively. The prevalence of hypoxemia among SCA participants was 47.1%. Prevalence of hypoxemia in males with SCA was 60.9% while 39.1% of the females had hypoxemia. Hypoxemia Sickle cell anaemia Steady state vaso-occlusive crisis Introduction Oxygen saturation (SaO 2 ) is the representative of percentage of oxygen occupied on the binding sites on haemoglobin [ 1 ]. Peripheral supply depends on effective oxygen transport to the tissue mitochondria, a critical task that is performed by haemoglobin [ 2 ]. Reduced oxygen saturation results in inadequate tissue supply, particularly when oxygen demand is increased, as occurs during exercise [ 3 ]. The (SaO 2 ) of less than or equal to 95% is called hypoxemia and it predicts a partial pressure of oxygen (PaO 2 ) of less than 70 mm Hg based on a normal oxyhaemoglobin curve [ 4 ]. Campbell and Colleagues reported significantly lower SaO 2 among adolescent with Hb SS when compared with Hb AA [ 5 ]. This was said to result from lung disease which lead to reduced gas exchange and alterations in the pulmonary vasculature or airways leading to ventilation-perfusion mismatching [ 5 ]. The significantly low SaO 2 among individuals with SCA was attributable to the chronic anaemic state, microvascular occlusion of the circulation by sickled erythrocytes and constant pertubation of the endothelial membrane with consequent elaboration of endothelial molecules which are commonly seen among SCA children especially those with various types of vaso-occlusive episodes[ 6 ]. Lower SaO 2 in people with SCA has also been reported to be associated with elevated serum lactate dehydrogenase, severe anaemia and reticulocytosis [ 7 , 8 , 9 ]. Previous studies among paediatric subjects have demonstrated haemoglobin desaturation with high prevalence of hypoxemia among children with sickle cell anaemia. With improved healthcare in this environment, the median survival of patients with SCA has risen, and therefore the prevalence of chronic organ diseases encountered in the adult population has also increased but only few studies have assessed the prevalence of hypoxemia among adult age group [ 10 ]. The study determined the level of hypoxemia among the SCA compared SPO 2 in young adults with SCA in steady state with age and sex matched individuals with Hb AA. Methods One hundred and thirty-six (67 males and 69 females) sickle cell anaemic individuals in steady state (group A) who were students of Obafemi Awolowo University, Ile-Ife, Nigeria participated in this study. The steady state was defined as absence of any crisis in the preceding 4 weeks and absence of any symptoms or signs attributable to acute illness [ 11 ]. The inclusion criteria for the Hb SS within the age range of 18–40 years and willingness to participate in the study. The exclusion criteria were presence of ongoing crisis/ within the last one month, pregnancy, blood transfusion in the last three months and alcohol intake/ smoking within the last 4 weeks. The control group were 86 (42 males and 44 females) apparently healthy young adults with Hb AA (group B) within the age range of 18–40 years who are age and sex-matched with group A, absence of systemic disease and willingness to participate in the study. The SaO 2 was determined using a pulse oximeter (ChoiceMMed TM ). Non-invasive measurement of SpO 2 was done by clipping the pulse oximeter to the left thumb after resting for five minutes in a thermoneutral environment. The SpO 2 and heart rate were recorded after stabilization of the reading for one minute. This measurement was done twice and the average was calculated. The average SpO 2 of less than or equal to 95% of was considered as hypoxemia. Results A total of 222 participants (136 Hb SS and 86 Hb AA) were recruited for this study. The mean ± SD age in years, SPO2 in % and pulse rate in beats per minutes of the Hb SS and Hb AA participants were 21.85 ± 3.04 and 22.14 ± 3.18 (t = 0.701, p = 0.436), 95.21 ± 3.02 and 98.07 ± 0.81 (t=-8.598, p < 0.0001) and 77.10 ± 9.28 and 73.16 ± 8.52 (t = 3.173, p = 0.002) respectively as shown in Table 1 . Sixty-four (47.1%) of the participants with Hb SS had hypoxemia while none of the Hb AA participants had hypoxemia. Out of the 69 females with Hb SS that participated in the study, 27 (39.1%) had hypoxemia while 37 (55.2%) out of 67 males had hypoxemia has shown in Table 2 . Table 1 Effect of Haemoglobin type on Oxygen Saturation and Pulse Rate Hb SS (n = 136) Hb AA (n = 86) T p-value Age (years) 21.85 ± 3.04 22.14 ± 3.18 -0.701 0.436 Oxygen Saturation (%) 95.21 ± 3.02 98.07 ± 081 -8.598 < 0.001* Pulse Rate (bpm) 77.10 ± 9.28 73.16 ± 8.52 3.173 0.002* *- significant p-value Table 2 Prevalence of Hypoxemia among Sickle Cell Anaemic Participants Hypoxemia Non-hypoxemia Male (n = 67) 37 (55.2%) 30 (44.8%) Female (n = 69) 27 (39.1%) 42 (60.9%) Total (n = 136) 64 (47.1%) 72 (52.9%) Hypoxemia – SPO2 ≤ 95%, Non-hypoxemia – SPO2 > 95% χ 2 − 3.534, p-value – 0.061 Discussion The mean SPO 2 of 95.21% among SCA observed in this study was similar to 95.5% reported by Ladu et al among sickle cell individuals within the same age range and was significantly lower among the participants with SCA than the control [ 10 ]. These findings were attributed to recurrent episodes of acute chest syndrome which result in a sequalae of irreversible chronic lung disease that gave rise to defective oxygenation of blood even at steady state [ 12 ]. Also, the sickle cell haemoglobin S is known to have an inherent property of causing a rightward shift of the oxy-haemoglobin dissociation curve in an attempt to enhance oxygen delivery at the tissue level by raising level of 2,3-diphosphoglycerate in SCA [ 13 , 14 ]. The pulmonary function abnormality is as a result of membrane diffusion defects, intra pulmonary right-left shunts and shift of Hb oxygen dissociation curve to the right of normal [ 14 ]. The high prevalence (47.1%) of hypoxemia gotten from this study among the participants with SCA was due to decrease in arterial blood oxygen content, oxygen carrying capacity from chronic anaemia and oxyhaemoglobin desaturation, in individuals with SCA [ 15 ]. This prevalence of hypoxemia observed in this study was greater than 13% recorded by Chinawa et al . in a study done among the young age group between 6 months and 18 years [ 16 ]. This is attributable to the chronic anaemic state and micro-vascular occlusion of the circulation by sickled red blood cells and pulmonary complications from recurrent sickling that is commoner with increasing age. This study also showed that the prevalence of hypoxemia was very high (55.2%) among male though not statistically significant when compared to 39.1% gotten among the female participants with SCA. The effect of gender on the SaO 2 among SCA was first discussed by Chinawa and Colleagues in 2013 which was not also significant. The reason was attributed to a transcription factor for haemoglobin F and Endothelial B receptor (ETBR) which was linked to X chromosome [ 17 ]. This receptor was said to be important in the body’s internal ability to control pain by releasing endorphins. Males were known to have less ETBR when compared to the females. Secondly, females were also said to have higher oxygen delivery to the tissues and hence there is minimal tissue damage in females during vaso‑occlusive crises [ 18 ]. The reason was poor understood but could be due to the smooth muscle relaxing effect of oestrogen. In conclusion, this study showed that the prevalence of hypoxemia occurs in close to half of the participants with SCA in steady state. Also, more half (55.2%) of the males with SCA have hypoxemia. It is hereby recommended that individual's steady-state oxygen saturation value is important in the interpretation of low values during acute complications. Declarations Authors’ contributions AMA, BRA and OO contributed to conception and design of the study. AMA, OO, AMS and AIO obtained the data, analysed and interpreted. AMA, AMS and OO drafted the original manuscript. AMA, AIO, AMS, BRA and OO critically revised the manuscript. All authors read and approved the final manuscript. Ethical approval and consent to participate Ethical approval was obtained from Ethics and Research Committee, Institute of Public Health, Obafemi Awolowo University Ile-Ife, Nigeria and informed consent was obtained from each participant. The experiment was performed in accordance with standard guidelines and regulations. Consent for publication Not applicable Availability of data and materials The datasets used and/or analysed during the current study available from the corresponding author on reasonable request. Funding No fund was received for carrying out this research. Competing interests The authors declare that they have no competing interests. References Pianosi P, Charge TD, Esseltine DW, Coates AL. Pulse oximetry in sickle cell disease. Archieves of Disease in Childhood. 1993;68(6):735–8. Neder JA, Nery LE, editors. editors. Fisiologia clínica do exercício: teoria e prática. São Paulo: Artes Médicas;; 2004. Ramos RP. How can anaemia negatively influence gas exchange? J Brasileiro de Pneumologia. 2017;43(1):1–2. Rackoff WR, Kunkel N, Silber JH, Asakura T, Ohene-Frempong K. Pulse oximetry and factors associated with hemoglobin oxygen desaturation in children with sickle cell disease. Blood. 1993;81:3422–7. Campbell A, Minniti CP, Nouraie M, Arteta M, Rana S, Onyekwere O, Sable C. Prospective evaluation of haemoglobin oxygen saturation at rest and after exercise in paediatric sickle cell disease patients. Br J Haematol. 2009;147(3):352–9. Ataga KI, Moore CG, Hillery CA, Jones S, Whinna HC, Strayham A. Coagulation activation and inflammation in sickle cell diseaseassociated pulmonary hypertension. Haematologica. 2008;93:20–6. Setty BN, Stuart MJ, Dampier C, Brodecki D, Allen JL. Hypoxaemia in sickle cell disease: biomarker modulation and relevance to pathophysiology. Lancet. 2003;362:1450–5. Quinn CT, Ahmad N. Clinical correlates of steady-state oxyhaemoglobin desaturation in children who have sickle cell disease. Br J Haematol. 2005;131:129–34. Kato GJ, McGowan V, Machado RF, Little JA, Taylor J 6th, Morris CR, Nichols JS, Wang X, Poljakovic M, Morris SM Jr, Gladwin MT. Lactate dehydrogenase as a biomarker of hemolysis associated nitric oxide resistance, priapism, leg ulceration, pulmonary hypertension, and death in patients with sickle cell disease. Blood. 2006;107(2):2279–85. Ladu AI, Abba AM, Bukar AA, Abulfathi FA, Kundili Y, Talba HA, et al. Assessment of Oxygen Saturaton Using Pulse Oximetry in Patents with Steady State HbSS. Annals of Clinical and Laboratory Research. 2018;6(2):237. Oguanobi NI, Ejim CE, Anisiuba BC, Onwubere BJC, Ike SO, Ibegbulam OG, Agwu O. Clinical and Electrocardiographic Evaluation of Sickle-Cell Anaemia Patients with Pulmonary Hypertension. International Scholarly Research Network, Haematology; 2012; 2012: 1–12. Ortiz FO, Aldrich TK, Nagel RL, Benjamin LJ. Accuracy of pulse oximetry in sickle cell disease. Am J Respir Crit Care Med. 2012;159:447–51. Seakins M, Bigs WN, Milner PF, Bertles JF. Erythrocyte Hb-S concentraton: An important factor in the low oxygen afinity of blood in sickle cell anemia. J Clin Invest. 1973;52:422–9. Rodgers GP. Overview of pathophysiology and rationale for treatment of sickle cell aenemia. Semin Hematol. 1997;34:2–7. Caboot JB, Allen JL. Hypoxemia in sickle cell disease: signifcance and management. Pediatr Respiratory Rev. 2014;15(1):17–23. Chinawa JM, Ubesie A, Chukwu BF, Ikefuna AN, Emodi IJ. Prevalence of hypoxemia among children with sickle cell anemia during steady state and crises: A cross-sectional study. Nigeria J Clin Pract. 2013;16:91–5. Wang WC. Sickle cell anaemia and other sickling syndromes. In: Green JP, Forester J, Lukens JN, editors. Wintrobes clinical haematolgy. Philadelphia: Lippincott Williams and Wilkins; 2004. pp. 1263–311. Ibia EO. Studies on physical growth status of sickle cell anaemia children seen in Calabar (Dissertation). Lagos, Nigeria: African college of physician; 1991. Additional Declarations No competing interests reported. Cite Share Download PDF Status: Published Journal Publication published 08 Apr, 2024 Read the published version in BMC Research Notes → Version 1 posted Editorial decision: Major revision 12 Oct, 2023 Reviews received at journal 12 Oct, 2023 Reviews received at journal 19 Sep, 2023 Reviewers agreed at journal 07 Sep, 2023 Reviewers agreed at journal 04 Sep, 2023 Reviewers invited by journal 04 Sep, 2023 Editor invited by journal 25 Jul, 2023 Editor assigned by journal 07 Jul, 2023 Submission checks completed at journal 07 Jul, 2023 First submitted to journal 03 Jul, 2023 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-3135169","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Short Report","associatedPublications":[],"authors":[{"id":216500924,"identity":"477ff2ee-88c5-4c68-8bbd-96c6d5c851a6","order_by":0,"name":"Muritala A. 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Peripheral supply depends on effective oxygen transport to the tissue mitochondria, a critical task that is performed by haemoglobin [\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e]. Reduced oxygen saturation results in inadequate tissue supply, particularly when oxygen demand is increased, as occurs during exercise [\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e]. The (SaO\u003csub\u003e2\u003c/sub\u003e) of less than or equal to 95% is called hypoxemia and it predicts a partial pressure of oxygen (PaO\u003csub\u003e2\u003c/sub\u003e) of less than 70 mm Hg based on a normal oxyhaemoglobin curve [\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e]. Campbell and Colleagues reported significantly lower SaO\u003csub\u003e2\u003c/sub\u003e among adolescent with Hb SS when compared with Hb AA [\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e]. This was said to result from lung disease which lead to reduced gas exchange and alterations in the pulmonary vasculature or airways leading to ventilation-perfusion mismatching [\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e]. The significantly low SaO\u003csub\u003e2\u003c/sub\u003e among individuals with SCA was attributable to the chronic anaemic state, microvascular occlusion of the circulation by sickled erythrocytes and constant pertubation of the endothelial membrane with consequent elaboration of endothelial molecules which are commonly seen among SCA children especially those with various types of vaso-occlusive episodes[\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e]. Lower SaO\u003csub\u003e2\u003c/sub\u003e in people with SCA has also been reported to be associated with elevated serum lactate dehydrogenase, severe anaemia and reticulocytosis [\u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e, \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e, \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e]. Previous studies among paediatric subjects have demonstrated haemoglobin desaturation with high prevalence of hypoxemia among children with sickle cell anaemia. With improved healthcare in this environment, the median survival of patients with SCA has risen, and therefore the prevalence of chronic organ diseases encountered in the adult population has also increased but only few studies have assessed the prevalence of hypoxemia among adult age group [\u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e]. The study determined the level of hypoxemia among the SCA compared SPO\u003csub\u003e2\u003c/sub\u003e in young adults with SCA in steady state with age and sex matched individuals with Hb AA.\u003c/p\u003e"},{"header":"Methods","content":"\u003cp\u003e One hundred and thirty-six (67 males and 69 females) sickle cell anaemic individuals in steady state (group A) who were students of Obafemi Awolowo University, Ile-Ife, Nigeria participated in this study. The steady state was defined as absence of any crisis in the preceding 4 weeks and absence of any symptoms or signs attributable to acute illness [\u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e]. The inclusion criteria for the Hb SS within the age range of 18\u0026ndash;40 years and willingness to participate in the study. The exclusion criteria were presence of ongoing crisis/ within the last one month, pregnancy, blood transfusion in the last three months and alcohol intake/ smoking within the last 4 weeks. The control group were 86 (42 males and 44 females) apparently healthy young adults with Hb AA (group B) within the age range of 18\u0026ndash;40 years who are age and sex-matched with group A, absence of systemic disease and willingness to participate in the study. The SaO\u003csub\u003e2\u003c/sub\u003e was determined using a pulse oximeter (ChoiceMMed\u003csub\u003eTM\u003c/sub\u003e). Non-invasive measurement of SpO\u003csub\u003e2\u003c/sub\u003e was done by clipping the pulse oximeter to the left thumb after resting for five minutes in a thermoneutral environment. The SpO\u003csub\u003e2\u003c/sub\u003e and heart rate were recorded after stabilization of the reading for one minute. This measurement was done twice and the average was calculated. The average SpO\u003csub\u003e2\u003c/sub\u003e of less than or equal to 95% of was considered as hypoxemia.\u003c/p\u003e"},{"header":"Results","content":"\u003cp\u003eA total of 222 participants (136 Hb SS and 86 Hb AA) were recruited for this study. The mean\u0026thinsp;\u0026plusmn;\u0026thinsp;SD age in years, SPO2 in % and pulse rate in beats per minutes of the Hb SS and Hb AA participants were 21.85\u0026thinsp;\u0026plusmn;\u0026thinsp;3.04 and 22.14\u0026thinsp;\u0026plusmn;\u0026thinsp;3.18 (t\u0026thinsp;=\u0026thinsp;0.701, p\u0026thinsp;=\u0026thinsp;0.436), 95.21\u0026thinsp;\u0026plusmn;\u0026thinsp;3.02 and 98.07\u0026thinsp;\u0026plusmn;\u0026thinsp;0.81 (t=-8.598, p\u0026thinsp;\u0026lt;\u0026thinsp;0.0001) and 77.10\u0026thinsp;\u0026plusmn;\u0026thinsp;9.28 and 73.16\u0026thinsp;\u0026plusmn;\u0026thinsp;8.52 (t\u0026thinsp;=\u0026thinsp;3.173, p\u0026thinsp;=\u0026thinsp;0.002) respectively as shown in Table \u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e. Sixty-four (47.1%) of the participants with Hb SS had hypoxemia while none of the Hb AA participants had hypoxemia. Out of the 69 females with Hb SS that participated in the study, 27 (39.1%) had hypoxemia while 37 (55.2%) out of 67 males had hypoxemia has shown in Table \u003cspan refid=\"Tab2\" class=\"InternalRef\"\u003e2\u003c/span\u003e.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab1\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eEffect of Haemoglobin type on Oxygen Saturation and Pulse Rate\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"5\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\"\u0026plusmn;\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\"\u0026plusmn;\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eHb SS (n\u0026thinsp;=\u0026thinsp;136)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eHb AA (n\u0026thinsp;=\u0026thinsp;86)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003eT\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c5\"\u003e \u003cp\u003ep-value\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eAge (years)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c2\"\u003e \u003cp\u003e21.85\u0026thinsp;\u0026plusmn;\u0026thinsp;3.04\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c3\"\u003e \u003cp\u003e22.14\u0026thinsp;\u0026plusmn;\u0026thinsp;3.18\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e-0.701\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e0.436\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eOxygen Saturation (%)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c2\"\u003e \u003cp\u003e95.21\u0026thinsp;\u0026plusmn;\u0026thinsp;3.02\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c3\"\u003e \u003cp\u003e98.07\u0026thinsp;\u0026plusmn;\u0026thinsp;081\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e-8.598\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e\u0026lt;\u0026thinsp;0.001*\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003ePulse Rate (bpm)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c2\"\u003e \u003cp\u003e77.10\u0026thinsp;\u0026plusmn;\u0026thinsp;9.28\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c3\"\u003e \u003cp\u003e73.16\u0026thinsp;\u0026plusmn;\u0026thinsp;8.52\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e3.173\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e0.002*\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003ctfoot\u003e \u003ctr\u003e\u003ctd colspan=\"5\"\u003e*- significant p-value\u003c/td\u003e\u003c/tr\u003e \u003c/tfoot\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab2\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 2\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003e\u003cb\u003ePrevalence of Hypoxemia among Sickle Cell Anaemic Participants\u003c/b\u003e\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"3\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eHypoxemia\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eNon-hypoxemia\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eMale (n\u0026thinsp;=\u0026thinsp;67)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e37 (55.2%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e30 (44.8%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eFemale (n\u0026thinsp;=\u0026thinsp;69)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e27 (39.1%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e42 (60.9%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eTotal (n\u0026thinsp;=\u0026thinsp;136)\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e64 (47.1%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e72 (52.9%)\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003ctfoot\u003e \u003ctr\u003e\u003ctd colspan=\"3\"\u003eHypoxemia \u0026ndash; SPO2\u0026thinsp;\u0026le;\u0026thinsp;95%, Non-hypoxemia \u0026ndash; SPO2\u0026thinsp;\u0026gt;\u0026thinsp;95%\u003c/td\u003e\u003c/tr\u003e \u003ctr\u003e\u003ctd colspan=\"3\"\u003eχ\u003csup\u003e2\u003c/sup\u003e \u0026minus;\u0026thinsp;3.534, p-value \u0026ndash; 0.061\u003c/td\u003e\u003c/tr\u003e \u003c/tfoot\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e"},{"header":"Discussion","content":"\u003cp\u003eThe mean SPO\u003csub\u003e2\u003c/sub\u003e of 95.21% among SCA observed in this study was similar to 95.5% reported by Ladu \u003cem\u003eet al\u003c/em\u003e among sickle cell individuals within the same age range and was significantly lower among the participants with SCA than the control [\u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e]. These findings were attributed to recurrent episodes of acute chest syndrome which result in a sequalae of irreversible chronic lung disease that gave rise to defective oxygenation of blood even at steady state [\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e]. Also, the sickle cell haemoglobin S is known to have an inherent property of causing a rightward shift of the oxy-haemoglobin dissociation curve in an attempt to enhance oxygen delivery at the tissue level by raising level of 2,3-diphosphoglycerate in SCA [\u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e13\u003c/span\u003e, \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eThe pulmonary function abnormality is as a result of membrane diffusion defects, intra pulmonary right-left shunts and shift of Hb oxygen dissociation curve to the right of normal [\u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e]. The high prevalence (47.1%) of hypoxemia gotten from this study among the participants with SCA was due to decrease in arterial blood oxygen content, oxygen carrying capacity from chronic anaemia and oxyhaemoglobin desaturation, in individuals with SCA [\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e]. This prevalence of hypoxemia observed in this study was greater than 13% recorded by Chinawa \u003cem\u003eet al\u003c/em\u003e. in a study done among the young age group between 6 months and 18 years [\u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e16\u003c/span\u003e]. This is attributable to the chronic anaemic state and micro-vascular occlusion of the circulation by sickled red blood cells and pulmonary complications from recurrent sickling that is commoner with increasing age.\u003c/p\u003e \u003cp\u003eThis study also showed that the prevalence of hypoxemia was very high (55.2%) among male though not statistically significant when compared to 39.1% gotten among the female participants with SCA. The effect of gender on the SaO\u003csub\u003e2\u003c/sub\u003e among SCA was first discussed by Chinawa and Colleagues in 2013 which was not also significant. The reason was attributed to a transcription factor for haemoglobin F and Endothelial B receptor (ETBR) which was linked to X chromosome [\u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e]. This receptor was said to be important in the body\u0026rsquo;s internal ability to control pain by releasing endorphins. Males were known to have less ETBR when compared to the females. Secondly, females were also said to have higher oxygen delivery to the tissues and hence there is minimal tissue damage in females during vaso‑occlusive crises [\u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e18\u003c/span\u003e]. The reason was poor understood but could be due to the smooth muscle relaxing effect of oestrogen.\u003c/p\u003e \u003cp\u003eIn conclusion, this study showed that the prevalence of hypoxemia occurs in close to half of the participants with SCA in steady state. Also, more half (55.2%) of the males with SCA have hypoxemia. It is hereby recommended that individual's steady-state oxygen saturation value is important in the interpretation of low values during acute complications.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eAuthors\u0026rsquo; contributions\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eAMA, BRA and OO contributed to conception and design of the study. AMA, OO, AMS and AIO obtained the data, analysed and interpreted. AMA, AMS and OO drafted the original manuscript. AMA, AIO, AMS, BRA and OO critically revised the manuscript. All authors\u0026nbsp;read and approved the final manuscript.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eEthical approval and consent to participate\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eEthical approval was obtained from Ethics and Research Committee, Institute of Public Health, Obafemi Awolowo University Ile-Ife, Nigeria and informed consent was obtained from each participant. The experiment was performed in accordance with standard guidelines and regulations.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConsent for publication\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eNot applicable\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAvailability of data and materials\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe datasets used and/or analysed during the current study available from the corresponding author on reasonable request.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eNo fund was received for carrying out this research.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eCompeting interests\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors declare that they have no competing interests.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003ePianosi P, Charge TD, Esseltine DW, Coates AL. Pulse oximetry in sickle cell disease. Archieves of Disease in Childhood. 1993;68(6):735\u0026ndash;8.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eNeder JA, Nery LE, editors. editors. Fisiologia cl\u0026iacute;nica do exerc\u0026iacute;cio: teoria e pr\u0026aacute;tica. S\u0026atilde;o Paulo: Artes M\u0026eacute;dicas;; 2004.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eRamos RP. How can anaemia negatively influence gas exchange? J Brasileiro de Pneumologia. 2017;43(1):1\u0026ndash;2.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eRackoff WR, Kunkel N, Silber JH, Asakura T, Ohene-Frempong K. Pulse oximetry and factors associated with hemoglobin oxygen desaturation in children with sickle cell disease. Blood. 1993;81:3422\u0026ndash;7.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eCampbell A, Minniti CP, Nouraie M, Arteta M, Rana S, Onyekwere O, Sable C. Prospective evaluation of haemoglobin oxygen saturation at rest and after exercise in paediatric sickle cell disease patients. Br J Haematol. 2009;147(3):352\u0026ndash;9.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eAtaga KI, Moore CG, Hillery CA, Jones S, Whinna HC, Strayham A. Coagulation activation and inflammation in sickle cell diseaseassociated pulmonary hypertension. Haematologica. 2008;93:20\u0026ndash;6.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSetty BN, Stuart MJ, Dampier C, Brodecki D, Allen JL. Hypoxaemia in sickle cell disease: biomarker modulation and relevance to pathophysiology. Lancet. 2003;362:1450\u0026ndash;5.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eQuinn CT, Ahmad N. Clinical correlates of steady-state oxyhaemoglobin desaturation in children who have sickle cell disease. Br J Haematol. 2005;131:129\u0026ndash;34.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eKato GJ, McGowan V, Machado RF, Little JA, Taylor J 6th, Morris CR, Nichols JS, Wang X, Poljakovic M, Morris SM Jr, Gladwin MT. Lactate dehydrogenase as a biomarker of hemolysis associated nitric oxide resistance, priapism, leg ulceration, pulmonary hypertension, and death in patients with sickle cell disease. Blood. 2006;107(2):2279\u0026ndash;85.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eLadu AI, Abba AM, Bukar AA, Abulfathi FA, Kundili Y, Talba HA, et al. Assessment of Oxygen Saturaton Using Pulse Oximetry in Patents with Steady State HbSS. Annals of Clinical and Laboratory Research. 2018;6(2):237.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eOguanobi NI, Ejim CE, Anisiuba BC, Onwubere BJC, Ike SO, Ibegbulam OG, Agwu O. Clinical and Electrocardiographic Evaluation of Sickle-Cell Anaemia Patients with Pulmonary Hypertension. International Scholarly Research Network, Haematology; 2012; 2012: 1\u0026ndash;12.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eOrtiz FO, Aldrich TK, Nagel RL, Benjamin LJ. Accuracy of pulse oximetry in sickle cell disease. Am J Respir Crit Care Med. 2012;159:447\u0026ndash;51.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSeakins M, Bigs WN, Milner PF, Bertles JF. Erythrocyte Hb-S concentraton: An important factor in the low oxygen afinity of blood in sickle cell anemia. J Clin Invest. 1973;52:422\u0026ndash;9.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eRodgers GP. Overview of pathophysiology and rationale for treatment of sickle cell aenemia. Semin Hematol. 1997;34:2\u0026ndash;7.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eCaboot JB, Allen JL. Hypoxemia in sickle cell disease: signifcance and management. Pediatr Respiratory Rev. 2014;15(1):17\u0026ndash;23.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eChinawa JM, Ubesie A, Chukwu BF, Ikefuna AN, Emodi IJ. Prevalence of hypoxemia among children with sickle cell anemia during steady state and crises: A cross-sectional study. Nigeria J Clin Pract. 2013;16:91\u0026ndash;5.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eWang WC. Sickle cell anaemia and other sickling syndromes. In: Green JP, Forester J, Lukens JN, editors. Wintrobes clinical haematolgy. Philadelphia: Lippincott Williams and Wilkins; 2004. pp. 1263\u0026ndash;311.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eIbia EO. Studies on physical growth status of sickle cell anaemia children seen in Calabar (Dissertation). Lagos, Nigeria: African college of physician; 1991.\u003c/span\u003e\u003c/li\u003e\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"bmc-research-notes","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"resn","sideBox":"Learn more about [BMC Research Notes](http://bmcresnotes.biomedcentral.com)","snPcode":"","submissionUrl":"https://www.editorialmanager.com/resn/default.aspx","title":"BMC Research Notes","twitterHandle":"@BMC_series","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"em","reportingPortfolio":"BMC Series","inReviewEnabled":true,"inReviewRevisionsEnabled":true},"keywords":"Hypoxemia, Sickle cell anaemia, Steady state, vaso-occlusive crisis","lastPublishedDoi":"10.21203/rs.3.rs-3135169/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-3135169/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003ch2\u003eObjectives\u003c/h2\u003e \u003cp\u003eHypoxia is a known feature of sickle cell anaemia (SCA) which results from chronic anaemia and recurrent vaso-occlusive crisis which can cause tissue ischaemia that leads to an end organ damage. The hallmark of SCA is chronic anaemia and recurrent vaso-occlusive crisis. The aim of this study is to compare the oxygen saturation of sickle cell anaemic individuals with the normal haemoglobin type (Hb AA) control and also to determine the prevalence of hypoxemia among SCA.\u003c/p\u003e\u003ch2\u003eResults\u003c/h2\u003e \u003cp\u003eTwo-hundred and twenty-two (136 Hb SS and 86 Hb AA) participated in the study. The mean\u0026thinsp;\u0026plusmn;\u0026thinsp;SD of age (years), oxygen saturation (%) and pulse rate (bpm) of participants with sickle cell anaemia and Hb AA control were 21.85\u0026thinsp;\u0026plusmn;\u0026thinsp;3.04 and 22.14\u0026thinsp;\u0026plusmn;\u0026thinsp;3.18 (t\u0026thinsp;=\u0026thinsp;0.701, p\u0026thinsp;=\u0026thinsp;0.436), 95.21\u0026thinsp;\u0026plusmn;\u0026thinsp;3.02 and 98.07\u0026thinsp;\u0026plusmn;\u0026thinsp;0.81 (t=-8.598, p\u0026thinsp;\u0026lt;\u0026thinsp;0.0001) and 77.10\u0026thinsp;\u0026plusmn;\u0026thinsp;9.28 and 73.16\u0026thinsp;\u0026plusmn;\u0026thinsp;8.52 (t\u0026thinsp;=\u0026thinsp;3.173, p\u0026thinsp;=\u0026thinsp;0.002) respectively. The prevalence of hypoxemia among SCA participants was 47.1%. Prevalence of hypoxemia in males with SCA was 60.9% while 39.1% of the females had hypoxemia.\u003c/p\u003e","manuscriptTitle":"Assessment of Hypoxemia among Young Adults with Sickle Cell Anaemia in Steady State: A cross‑sectional study","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2023-07-12 11:12:49","doi":"10.21203/rs.3.rs-3135169/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"decision","content":"Major revision","date":"2023-10-12T13:06:21+00:00","index":"","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2023-10-12T12:37:45+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2023-09-19T19:44:48+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"6a6a854e-4a6a-4800-b4e6-91d861468f6e","date":"2023-09-07T16:54:41+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"5f4de6c4-2e65-4b92-b770-118624156502","date":"2023-09-04T17:13:15+00:00","index":"hide","fulltext":""},{"type":"reviewersInvited","content":"","date":"2023-09-04T15:59:56+00:00","index":"","fulltext":""},{"type":"editorInvited","content":"","date":"2023-07-25T14:48:44+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2023-07-07T05:16:33+00:00","index":"","fulltext":""},{"type":"checksComplete","content":"","date":"2023-07-07T05:16:33+00:00","index":"","fulltext":""},{"type":"submitted","content":"BMC Research Notes","date":"2023-07-03T10:17:32+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"bmc-research-notes","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"resn","sideBox":"Learn more about [BMC Research Notes](http://bmcresnotes.biomedcentral.com)","snPcode":"","submissionUrl":"https://www.editorialmanager.com/resn/default.aspx","title":"BMC Research Notes","twitterHandle":"@BMC_series","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"em","reportingPortfolio":"BMC Series","inReviewEnabled":true,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"ded23e79-8a08-4084-8296-a38c55dc28df","owner":[],"postedDate":"July 12th, 2023","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[],"tags":[],"updatedAt":"2024-04-15T15:11:43+00:00","versionOfRecord":{"articleIdentity":"rs-3135169","link":"https://doi.org/10.1186/s13104-024-06765-0","journal":{"identity":"bmc-research-notes","isVorOnly":false,"title":"BMC Research Notes"},"publishedOn":"2024-04-08 15:00:44","publishedOnDateReadable":"April 8th, 2024"},"versionCreatedAt":"2023-07-12 11:12:49","video":"","vorDoi":"10.1186/s13104-024-06765-0","vorDoiUrl":"https://doi.org/10.1186/s13104-024-06765-0","workflowStages":[]},"version":"v1","identity":"rs-3135169","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-3135169","identity":"rs-3135169","version":["v1"]},"buildId":"7rjqhiLT3MXkJMwkYKINL","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}

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