Validation of noninvasive photoacoustic measurements of sagittal sinus oxyhemoglobin saturation in hypoxic neonatal piglets

Jeeun Kang, Emad Boctor, Shawn Adams, Ewa Kulikowicz, Haichong K. Zhang, Raymond C Koehler, Ernest M Graham

Research output: Contribution to journalArticle

Abstract

We hypothesize that noninvasive photoacoustic imaging can accurately measure cerebral venous oxyhemoglobin saturation (SO2) in a neonatal model of hypoxia-ischemia. In neonatal piglets, which have a skull thicknes.comparable to that of human neonates, w.compared the photoacoustic measurement of sagittal sinus SO2 against that measured directly by blood sampling over a wide range of conditions. Systemic hypoxia was produced by decreasing inspired oxygen stepwise (i.e., 100, 21, 19, 17, 15, 14, 13, 12, 11, and 10%) with and without unilateral or bilateral ligation of th.common carotid arteries to enhance hypoxiaischemia. Transcranial photoacoustic sensing enabled us to detect changes in sagittal sinus O2 saturation throughout the tested range of 5-80% without physiologically relevant bias. Despite lower cortical perfusion and higher oxygen extraction in groups with carotid occlusion at equivalent inspired oxygen, photoacoustic measurements successfully provided a robust linear correlation that approached the line of identity with direct blood sample measurements. Receiver-operating characteristic analysis for discriminating SO2 <30% showed an area under the curve of 0.84 for the pooled group data, and 0.87, 0.91, and 0.92 for hypoxia alone, hypoxia plus unilateral occlusion, and hypoxia plus bilateral occlusion subgroups, respectively. The detection precision in this critical range was confirmed with sensitivity (87.0%), specificity (86.5%), accuracy (86.8%), positive predictive value (90.5%), and negative predictive value (81.8%) in th.combined dataset. These results validate the capability of photoacoustic sensing technology to accurately monitor sagittal sinus SO2 noninvasively over a wide range and support its use for early detection of neonatal hypoxia-ischemia. NEW & NOTEWORTHY We present data to validate the noninvasive photoacoustic measurement of sagittal sinus oxyhemoglobin saturation. In particular, this paper demonstrates the robustness of this methodology during a wide range of hemodynamic and physiological changes induced by the stepwise decrease of fractional inspired oxygen to produce hypoxia and by unilateral and bilateral ligation of th.common carotid arteries preceding hypoxia to produce hypoxiaischemia. This technique may be useful for diagnosing risk of neonatal hypoxic-ischemic encephalopathy.

Original languageEnglish (US)
Pages (from-to)983-989
Number of pages7
JournalJournal of Applied Physiology
Volume125
Issue number4
DOIs
StatePublished - Oct 1 2018

Fingerprint

Oxyhemoglobins
Oxygen
Common Carotid Artery
Ligation
Photoacoustic Techniques
Ischemia
Brain Hypoxia-Ischemia
Hypoxia
Skull
ROC Curve
Area Under Curve
Perfusion
Hemodynamics
Sensitivity and Specificity

Keywords

  • hypoxic-ischemic encephalopathy
  • neonate
  • oxygen saturation
  • photoacoustics
  • sagittal sinus

ASJC Scopus subject areas

  • Physiology
  • Physiology (medical)

Cite this

Validation of noninvasive photoacoustic measurements of sagittal sinus oxyhemoglobin saturation in hypoxic neonatal piglets. / Kang, Jeeun; Boctor, Emad; Adams, Shawn; Kulikowicz, Ewa; Zhang, Haichong K.; Koehler, Raymond C; Graham, Ernest M.

In: Journal of Applied Physiology, Vol. 125, No. 4, 01.10.2018, p. 983-989.

Research output: Contribution to journalArticle

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abstract = "We hypothesize that noninvasive photoacoustic imaging can accurately measure cerebral venous oxyhemoglobin saturation (SO2) in a neonatal model of hypoxia-ischemia. In neonatal piglets, which have a skull thicknes.comparable to that of human neonates, w.compared the photoacoustic measurement of sagittal sinus SO2 against that measured directly by blood sampling over a wide range of conditions. Systemic hypoxia was produced by decreasing inspired oxygen stepwise (i.e., 100, 21, 19, 17, 15, 14, 13, 12, 11, and 10{\%}) with and without unilateral or bilateral ligation of th.common carotid arteries to enhance hypoxiaischemia. Transcranial photoacoustic sensing enabled us to detect changes in sagittal sinus O2 saturation throughout the tested range of 5-80{\%} without physiologically relevant bias. Despite lower cortical perfusion and higher oxygen extraction in groups with carotid occlusion at equivalent inspired oxygen, photoacoustic measurements successfully provided a robust linear correlation that approached the line of identity with direct blood sample measurements. Receiver-operating characteristic analysis for discriminating SO2 <30{\%} showed an area under the curve of 0.84 for the pooled group data, and 0.87, 0.91, and 0.92 for hypoxia alone, hypoxia plus unilateral occlusion, and hypoxia plus bilateral occlusion subgroups, respectively. The detection precision in this critical range was confirmed with sensitivity (87.0{\%}), specificity (86.5{\%}), accuracy (86.8{\%}), positive predictive value (90.5{\%}), and negative predictive value (81.8{\%}) in th.combined dataset. These results validate the capability of photoacoustic sensing technology to accurately monitor sagittal sinus SO2 noninvasively over a wide range and support its use for early detection of neonatal hypoxia-ischemia. NEW & NOTEWORTHY We present data to validate the noninvasive photoacoustic measurement of sagittal sinus oxyhemoglobin saturation. In particular, this paper demonstrates the robustness of this methodology during a wide range of hemodynamic and physiological changes induced by the stepwise decrease of fractional inspired oxygen to produce hypoxia and by unilateral and bilateral ligation of th.common carotid arteries preceding hypoxia to produce hypoxiaischemia. This technique may be useful for diagnosing risk of neonatal hypoxic-ischemic encephalopathy.",
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