Released this past November, the list is based on data collected from the Web of Science and highlights some of the world’s most influential scientific minds by naming the researchers whose publications over the previous decade have included a high number of Highly Cited Papers placing them among the top 1% most-cited.
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We wish to congratulate all of the researchers named and especially our authors on this amazing accomplishment! We are happy and proud to share in their success!
IntechOpen is proud to announce that 179 of our authors have made the Clarivate™ Highly Cited Researchers List for 2020, ranking them among the top 1% most-cited.
\n\n
Throughout the years, the list has named a total of 252 IntechOpen authors as Highly Cited. Of those researchers, 69 have been featured on the list multiple times.
\n\n\n\n
Released this past November, the list is based on data collected from the Web of Science and highlights some of the world’s most influential scientific minds by naming the researchers whose publications over the previous decade have included a high number of Highly Cited Papers placing them among the top 1% most-cited.
\n\n
We wish to congratulate all of the researchers named and especially our authors on this amazing accomplishment! We are happy and proud to share in their success!
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1. Introduction
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Brain death is defined as permanent cessation of all vital functions of the brain. It is principally established using clinical criteria including coma, absence of brain stem reflexes, and using apnea test. In Canada, two physicians must determine whether particular patient is brain dead or not [1, 2]. The criteria for declaring brain death includes deep unresponsive coma with established etiology, absence of reversible conditions [2]. Absence of brain stem reflexes includes absence of gag, cough, bilateral absence of corneal response, pupillary response to light and vestibule-ocular response, absence of respiratory efforts based on apnea test, and absence of confounding factors [2]. Ancillary imaging tests are necessary in situations when neurological examination or the apnea test cannot be performed or its validity comes into a question [3]. These situations include when patients have resuscitated shock, hypothermia, severe metabolic abnormalities, complex spinal reflexes, peripheral nerve or muscular dysfunctions, high cervical spine injury, craniofacial trauma or if the patient is on sedative drugs such as alcohol, barbiturates, sedatives, and hypnotics.
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An ideal ancillary test should not have any false positive results. This is very important in brain death patients. If the ancillary test confirms death, when in fact, patient is not dead, is very dangerous and raises critical social, ethical and legal concerns. The main objective of the ancillary test would be to demonstrate the absence of cerebral electric activity or cerebral circulatory arrest [4]. Based on this, the first type assesses the electrical functions of the brain, and the other type analyses cerebral blood flow in the brain on imaging. Here, we provide description of cerebral blood flow imaging techniques and compare them.
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2. Characteristics of ideal ancillary test for determining the brain death
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Young and his colleagues described the attributes of an ideal ancillary test [5]. A reliable ancillary test should meet all the criteria mentioned below.
When the test confirms brain death, there should be no one that recovers or have the potential to recover. There should be no false positives.
The test should be independently sufficient enough to establish whether brain death is present or not.
The test should not be susceptible to external or internal confounding factors such as drug effects and metabolic disturbances.
The test should have standardized technology, technique, and classification of results.
The test should be inexpensive, safe, and readily applied. Testing should not be restricted to only few tertiary academic centers. It could be applied with any intensive care unit, and the technique should be mastered without difficulty.
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3. Ancillary imaging tests used in brain death determination
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3.1 Digital subtraction angiography (DSA)
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This is considered the gold standard for ancillary imaging test. DSA is the first used modality for determining the cerebral blood flow. It is typically performed with a catheter tip in the aortic arch and contrast injection into each of the four arteries supplying the brain [3]. At least two injections, 20 min apart, must show an absence of filling of four arteries as their course becomes intracranial (Figure 1) [3, 6].
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Figure 1.
Digital subtraction angiography image of a brain dead patient showing no intracranial filling on selective (A) left and (B) right common carotid artery as well as (C) left and (D) right vertebral artery angiograms. These show continued filling of the extracranial arteries including (A) left and (B) right external carotid arteries.
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This test is capable of detecting dynamic blood flow in the arteries, veins, and capillaries. The criteria for brain death diagnosis using this method include no intracerebral filling at the level of entry into the skull of carotid or vertebral artery and filling of external carotid arteries. But this method does not have the spatial resolution to distinguish the blood flow in the different parts of the brain such as brainstem. Other disadvantages include transportation of patents to the angio suite; requires expert operator to perform; is invasive; and requires injection of contrast medium that may have a potential risk to the patients with kidney diseases. It can have “stasis filling” due to diffusion of contrast in the static column of blood, which can result in false negatives. Thus, it is an expensive procedure and not readily available in many hospitals and may not be easy to interpret in many healthcare facilities.
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3.2 Nuclear scintigraphy
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This is another gold standard ancillary imaging test for determination of brain death. In this technique, a gamma emitting radioactive tracer is intravenously injected and is detected by a radio counter in the nuclear medicine. One of the radioactive tracers used is Tc99m-DTPA. After bolus intravenous injection of the tracer, brain vascular flow is estimated. DTPA does not have the ability to cross the intact blood brain barrier, so intracranial blood flow is seen in normal patients. However, Tc99m-DTPA tracer has low resolution for brain vascular flow [7]. There are two other radiopharmaceuticals, namely Tc99m-HMPAO (hexamethylpropyleneamine oxime) and Tc99m-ECD (ethyl cysteinate dimer) [8]. Both of them are brain specific, lipophilic and after intravenous injection, they cross the blood brain barrier. Because of this property, they are accumulated proportional to the blood flow in normal gray matter including brain cells of cerebrum, cerebellum, and brainstem [8]. So, it is not only blood flow but also brain parenchyma is seen in the normal functioning brain. In this method, radioactive isotope is injected 30 min after its reconstitution. Images are taken immediately after injection, after 30 min, and finally after 2 hours. If there is no blood flow, there is no accumulation of tracer in the brain and brain looks hollow, this phenomenon is known as “hollow skull” or “empty bulb” sign (Figure 2). These injected radioactive tracer compounds are safe to the patients because they do not interact with their medication and have no associated side effects [8].
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Figure 2.
“Hallow skull”/“empty bulb” sign shown in brain death patient using (A) AP and (B) lateral nuclear scintigraphy imaging. Flow and delayed imaging demonstrated no significant intracranial flow or parenchymal uptake.
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Disadvantages of this technique is sometimes posterior fossa may be difficult to visualize, and uptake may be affected by hypothermia and barbiturates [3]. It does not have the spatial resolution to detect isolated brainstem activity. Other disadvantages include associated time delay and availability of this technique. Nuclear scintigraphy requires instrumentation, an experienced radiologist to interpret the test results, and the radioactive tracer used in this test is expensive and requires a trained pharmacist to reconstitute.
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3.3 CT head
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Computed tomography (CT) was introduced in 1970, since then it has revolutionized the assessment of head injuries including brain death [9]. It is fast, readily available, and requires no contrast medium. It is a standard imaging test for the patients admitted in the hospital because of brain injuries. Plain head CT scan can visualize brain tissue and lesion. It accurately diagnoses skull fractures, intracranial bleeds, brain contusions, and brain herniation. For diagnosis of brain death, a diffuse loss of gray-white mater differentiation needs to be established (Figure 3).
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Figure 3.
Plain head CT image of a brain dead patient showing diffuse loss of gray-white mater differentiation.
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Plain head CT has several limitations in assessment of brain death. Plain head CT does not provide functional information of the brain and does not assess intracranial blood flow. Diffuse loss of gray-white mater differentiation is likely a late phenomenon and the inter-rater reliability is poor [10].
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Contrast enhanced CT of head can be acquired to assess brain blood flow but is delayed compared to CT angiography. Contrast-enhanced CT acquisition requires a delay of 5 min, whereas CT angiography requires only 12–16 seconds. This delay makes the contrast-enhanced CT highly susceptible to “stasis filling” of the brain blood vessels. Thus, plain head CT is not very reliable test in determining brain death.
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3.4 Computed tomography angiography (CTA)
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CTA is a valuable ancillary imaging technique for intracranial blood flow. CTA was first reported in 1998 as an ancillary test in diagnosing the brain death [11]. According to Dupas et al., in 14 patients who were diagnosed as brain dead using clinical criteria, the results were confirmed to have 100% sensitivity using CTA [11]. CTA is fast, non-invasive, technically noncomplicated, inexpensive, readily and widely available. It is perhaps the most widely available brain blood-flow test. CTA has a high spatiotemporal resolution and is relatively operator independent. Several European countries have adopted CTA as an ancillary test but not the United States [12, 13].
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The technique of CTA involves rapid intravenous administration of iodinated contrast followed by volume scanning of the whole brain. For imaging of brain death at least two acquisitions should be performed, 60 seconds apart [9]. Others have proposed at least three acquisitions-arterial phase scanning after 20 seconds and venous phase scanning after 50–60 seconds [4].
\n
Diagnostic criteria for brain death using CTA include lack of intracranial arterial contrast opacification. Lack of intracranial contrast opacification can be assessed by 4, 7, and 10 point scales. In 4 point scale, M4 (cortical) segments of middle cerebral artery (MCA) and intracerebral vein (ICV) are evaluated for contrast opacification [11]. The 7 point scale included evaluation of MCA-M4, anterior cerebral artery (ACA), ICV, and great cerebral vein (GCV) [14]. In the 10 point scale, all the seven segments of the 7 point scale plus posterior cerebral artery (PCA) and basilar artery are included [6]. In a recent study, Garret et al. assessed statistical performance of CTA in diagnosing brain death. For all the 18 patients included in the study, CTA had sensitivity of 75%, specificity of 100%, positive predictive value of 100%, and negative predictive value of 33% [15]. Another recent study from Macdonald et al. reported the diagnostic accuracy and inter-rater reliability of different ancillary imaging tests used for brain death in 74 patients. They showed that CTA along with CTP and radionuclide scan had a specificity and positive predictive value of 100% [10]. These results certainly add to the growing medical literature that supports the use of CTA as a reliable ancillary imaging test in confirming the brain death. However, systematic reviews do not support use of CTA as an ancillary imaging test for confirmation of brain death [16, 17].
\n
The disadvantages of CTA are that this is not widely available as a bedside test and patient needs to be transported to imaging facility and this is challenging for an intensive care unit (ICU) patient. However, this can be obviated by the use of portable CT scanners in the future. CTA provides incomplete quantitative measurement of cerebral blood flow due predominantly of “stasis filling” (Figure 4). It is defined as delayed, weak persistent opacification of proximal cerebral arteries. This phenomenon causes a major problem in the development of reliable CTA protocol for the diagnosis of brain death [6]. There is also potential risk of damage to the organs of the brain death patients because of iodinated contrast media used in CTA. However based on the volume of contrast used for CTA, this is rare or negligible [18, 19].
\n
Figure 4.
Axial CTA images (A, B) in patient with clinically confirmed brain death show contrast opacification of bilateral internal carotid arteries, proximal branches of bilateral middle, and anterior cerebral arteries. None of the two images show opacification of M4 or cortical branches of middle cerebral arteries, distal anterior cerebral artery (ACA), internal and great cerebral vein. There is some opacification of only right posterior cerebral artery. There is continued filling of the extra cranial arteries.
\n
\n
\n
3.5 Computed tomography perfusion (CTP)
\n
CTP is an advanced CT scan technique that provides both anatomical as well as functional information about the brain. CTP is useful in detecting perfusion even in small vessels such as arterioles, capillaries, and venules [20]. CTP is routinely used for evaluation of cerebral ischemia and vascularization of brain tumors and has the spatial resolution to quantify perfusion in any selected part of the brain [21, 22]. This imaging technique can help in calculation of cerebral blood flow (CBF) and cerebral blood volume (CBV). Normal CBF in the brain is 50–60 ml/100 mg/min and CTP can measure as low as 1.2 ml/100 mg/min [20]. CTP is very sensitive in detecting the blood flow and can detect decreased perfusion as low as 2–3% in CBF and 2% in CBV [23]. In CTP acquisition protocol, patients will undergo whole brain coverage with 80 kVp, 100 mAs resulting in a radiation dose of approximately CT dose index of 189.64 mGy [20]. A minimum scan duration of 60 seconds is recommended to reliably cover the venous phase of the circulation. A total of 40 ml nonionic iodinated contrast medium injected at the rate of 5 ml/seconds, followed by 40 ml of saline flush at the rate of 5 ml/seconds. Regular perfusion analysis is performed if intracranial arteries are seen on the source images [20]. Whole brain death could be seen as no intracranial CBF or CBV (Figure 5). Shankar et al. compared CTP and CTA derived from the CTP for confirmation of brain death in a retrospective review of 11 patients clinically suspected of brain death [20]. CTA showed a sensitivity of 72.7% for 7- and 4-point scales, 81.8% sensitivity for opacification of ICV, and 100% sensitivity for CTP scores in the brainstem [20]. They, for the first time, showed that CTP can be a valuable ancillary tool in early detection of brain death. Recently, Sawicki et al. tested the reliability and diagnostic accuracy of CTP over CTA in determining brain death [24]. For whole brain CTP, they also showed a sensitivity of 100% to confirm the diagnosis of brain death [24]. MacDonald et al. showed similar sensitivity [10].
\n
Figure 5.
CT perfusion showing no detectable cerebral blood flow (CBF) (A) and cerebral blood volume (CBV) (B) in the whole brain.
\n
CTP can also evaluate brain-stem specific CBF [10, 20]. The concept of isolated brainstem death was first proposed by Shankar et al. in clinically confirmed brain death patients (Figure 6) [20]. Exact pathophysiological mechanism behind isolated brainstem death is not yet known. This is described when in patients with clinically confirmed brain death, there is presence of blood flow in the supratentorial brain and isolated absence of blood flow in the brainstem [10, 20]. Clinical examination does not differentiate between whole brain death and isolated brainstem death. CTP is the first imaging test reported to show the phenomenon of isolated brainstem death [10, 20]. It is suspected that isolated brainstem death is an earlier phenomenon in the process of brain death and may help early declaration of brain death [10]. However, the concept of brainstem death is debatable at the present time, and more studies are needed to establish this phenomenon.
\n
Figure 6.
CT perfusion showing matched defect on cerebral blood flow (CBF) (A and B) and cerebral blood volume (CBV) (C and D) maps in brainstem only. The supratentorial brain as well as cerebellum showed preserved CBF and CBV.
\n
Like CTA, CTP is a widely available tool and with the availability of automated software, CTP is relatively operator-independent [20]. The advantage of CTP is that it can be performed along with CTA. CTP has a presumed risk of contrast induced renal damage in the patients with kidney disease. But, based on the volume of contrast used for CTP, the chances of nephrotoxicity is very rare or negligible [18, 19].
\n
\n
\n
3.6 Magnetic resonance imaging (MRI)
\n
It is a reliable high-resolution imaging of brain and has been used for imaging for brain death. MRI has an advantage of not requiring nephrotoxic contrast material for demonstration of cerebral blood flow. It is noninvasive and accurate in identifying structural abnormalities in the brain. Common MRI findings in brain death patients are variable edema, diffuse cortical high signal intensity, diffuse cerebral white matter injury, and tonsillar herniation [25, 26]. Lovblad and colleagues demonstrated the usefulness of diffusion weighted imaging (DWI) in the diagnosis of brain death [27]. They reported that apparent diffusion coefficient (ADC) values are reduced in brain death patients when compared to the normal individuals [27]. Using DWI and ADC mapping, it is possible to identify areas of cytotoxic damage and ischemic damage [4]. However, this has not been accepted in the imaging guidelines for brain death. The major disadvantages of this method are the length of the scan time and obtaining MRI on ventilated patients as they may have several contraindications to MRI.
\n
\n
\n
3.7 Magnetic resonance angiography (MRA)
\n
It is a reliable test for cerebral blood flow [28] and can detect intracranial arterial blood flow and flow voids (Figure 7). However, MRA has not yet been proven as an ancillary test in assessing the brain death. Time of flight MRA is relatively immune to “stasis filling” when compared to CTA or DSA. Like any MRI, the patient needs transportation to the radiology department, and the length of time for MRA is longer than that for CTA or CTP. There is requirement of having specialized critical care equipment in a scanner.
\n
Figure 7.
Time of flight MR angiography image of a brain dead patient showed no intracranial flow but preserved extracranial flow on source image (A), axial (B), and coronal (C) maximum intensity projection images.
\n
\n
\n
3.8 Magnetic resonance perfusion (MR perfusion)
\n
MRP is noninvasive and can be used to detect intracranial arterial blood flow. It can also detect perfusion parameters of affected brain tissues such as cerebral blood flow and cerebral blood volume. There are not many reports in the literature that used MR perfusion as an ancillary imaging tool, and more research studies are needed to establish the reliability of this technique in the clinical setting.
\n
\n
\n
\n
4. Conclusions
\n
For clinical confirmation of brain death, the three essential criteria are apnea, absence of brain stem reflexes, and coma. In situations where brain death cannot be confirmed by one of these clinical tests or there are uncertainties around the reliability of clinical examination, ancillary imaging techniques are required to confirm brain death. We describe different ancillary imaging tests commonly used and reported to confirm the brain death. More research is required to validate these tests to become gold standards in the clinical practice.
\n
\n
Conflict of interests
Jai Shankar is the co-PI of ongoing INDEX study for prospective evaluation of CT perfusion for confirmation of brain death.
\n',keywords:"brain death, ancillary imaging test, brainstem function, computed tomography, DSA, nuclear scintigraphy, CT perfusion (CTP), CT angiography (CTA), magnetic resonance imaging (MRI), magnetic resonance angiography (MRA), magnetic resonance perfusion (MRP)",chapterPDFUrl:"https://cdn.intechopen.com/pdfs/67894.pdf",chapterXML:"https://mts.intechopen.com/source/xml/67894.xml",downloadPdfUrl:"/chapter/pdf-download/67894",previewPdfUrl:"/chapter/pdf-preview/67894",totalDownloads:373,totalViews:0,totalCrossrefCites:0,totalDimensionsCites:0,hasAltmetrics:1,dateSubmitted:"January 28th 2019",dateReviewed:"April 24th 2019",datePrePublished:"June 27th 2019",datePublished:null,dateFinished:null,readingETA:"0",abstract:"Brain death is an irreversible termination of functions of the entire brain including brain stem. The American Association of Neurology has defined brain death with three cardinal criteria, namely cessation of the functions of brain including brain stem, coma or unresponsiveness, and apnea. Ancillary testing is done in situations where clinical criteria of brain death cannot be determined by neurological examination or by apnea test. Ancillary tests for determining brain death can be primarily divided into two groups. One group includes tests that can test brain’s electrical functions and the other group includes tests that can document cerebral blood flow in the brain on imaging. In this chapter, we present characteristics of the ideal ancillary test in the diagnosis of brain death and also describe various types of ancillary imaging tests used in the clinical setting for brain death determination and the merits and demerits associated with these techniques.",reviewType:"peer-reviewed",bibtexUrl:"/chapter/bibtex/67894",risUrl:"/chapter/ris/67894",book:{slug:"disorders-of-consciousness-a-review-of-important-issues"},signatures:"Sudharsana Rao Ande and Jai Jai Shiva Shankar",authors:null,sections:[{id:"sec_1",title:"1. Introduction",level:"1"},{id:"sec_2",title:"2. Characteristics of ideal ancillary test for determining the brain death",level:"1"},{id:"sec_3",title:"3. Ancillary imaging tests used in brain death determination",level:"1"},{id:"sec_3_2",title:"3.1 Digital subtraction angiography (DSA)",level:"2"},{id:"sec_4_2",title:"3.2 Nuclear scintigraphy",level:"2"},{id:"sec_5_2",title:"3.3 CT head",level:"2"},{id:"sec_6_2",title:"3.4 Computed tomography angiography (CTA)",level:"2"},{id:"sec_7_2",title:"3.5 Computed tomography perfusion (CTP)",level:"2"},{id:"sec_8_2",title:"3.6 Magnetic resonance imaging (MRI)",level:"2"},{id:"sec_9_2",title:"3.7 Magnetic resonance angiography (MRA)",level:"2"},{id:"sec_10_2",title:"3.8 Magnetic resonance perfusion (MR perfusion)",level:"2"},{id:"sec_12",title:"4. Conclusions",level:"1"},{id:"sec_16",title:"Conflict of interests",level:"1"}],chapterReferences:[{id:"B1",body:'\nHeran MKS, Heran NS, Shemie SD. A review of ancillary tests in evaluating brain death. Canadian Journal of Neurological Sciences. 2008;35(4):409-419\n'},{id:"B2",body:'\nShemie SD, Doig C, Dickens B, Byrne P, Wheelock B, Rocker G, et al. Severe brain injury to neurological determination of death: Canadian forum recommendations. Canadian Medical Association. 2006;174(6):S1-S13\n'},{id:"B3",body:'\nBusl KM, Greer DM. Pitfalls in the diagnosis of brain death. Neurocritical Care. 2009;11(2):276-287\n'},{id:"B4",body:'\nSawicki M, Wojczal J, Birkenfeld B, Cyrylowski L. Brain death imaging. In: Saba L, Raz E, editors. Neurovascular Imaging. New York, NY: Springer; 2014. pp. 1-33. Available from: http://link.springer.com/10.1007/978-1-4614-9212-2_26-1\n\n'},{id:"B5",body:'\nYoung GB, Shemie SD, Doig CJ, Teitelbaum J. Brief review: The role of ancillary tests in the neurological determination of death. Canadian Journal of Anesthesia. 2006;53(6):620-627\n'},{id:"B6",body:'\nSawicki M, Bohatyrewicz R, Safranow K, Walecka A, Walecki J, Rowinski O, et al. Dynamic evaluation of stasis filling phenomenon with computed tomography in diagnosis of brain death. Neuroradiology. 2013;55(9):1061-1069\n'},{id:"B7",body:'\nMunari M, Zucchetta P, Carollo C, Gallo F, De Nardin M, Marzola MC, et al. Confirmatory tests in the diagnosis of brain death: Comparison between SPECT and contrast angiography. Critical Care Medicine. 2005;33(9):2068-2073\n'},{id:"B8",body:'\nZuckier LS, Kolano J. Radionuclide studies in the determination of brain death: Criteria, concepts, and controversies. Seminars in Nuclear Medicine. 2008;38(4):262-273\n'},{id:"B9",body:'\nRosenblum ML, Hoff JT, Norman D, Weinstein PR, Pitts L. Decreased mortality from brain abscesses since advent of computerized tomography. Journal of Neurosurgery. 1978;49(5):658-668\n'},{id:"B10",body:'\nMacDonald D, Stewart-Perrin B, Shankar JJS. The role of neuroimaging in the determination of brain death. Journal of Neuroimaging. 2018;28(4):374-379\n'},{id:"B11",body:'\nDupas B, Gayet-Delacroix M, Villers D, Antonioli D, Veccherini MF, Soulillou JP. Diagnosis of brain death using two-phase spiral CT. American Journal of Neuroradiology. 1998;19(4):641-647\n'},{id:"B12",body:'\nWijdicks EFM. Brain death worldwide: Accepted fact but no global consensus in diagnostic criteria. Neurology. 2002;58(1):20-25\n'},{id:"B13",body:'\nBeltramello A, Casartelli Liviero M, Bernardi B, Causin F, Di Paola F, Muto M, et al. Computed tomography angiography: A double step methodology in brain death confirmation. Minerva Anestesiologica. 2014;80(7):862-863\n'},{id:"B14",body:'\nLeclerc X, Taschner CA, Vidal A, Strecker G, Savage J, Gauvrit JY, et al. The role of spiral CT for the assessment of the intracranial circulation in suspected brain-death. Journal of Neuroradiology. 2006;33(2):90-95\n'},{id:"B15",body:'\nGarrett MP, Williamson RW, Bohl MA, Bird CR, Theodore N. Computed tomography angiography as a confirmatory test for the diagnosis of brain death. Journal of Neurosurgery. 2018;128(2):639-644\n'},{id:"B16",body:'\nKramer AH, Roberts DJ. Computed tomography angiography in the diagnosis of brain death: A systematic review and meta-analysis. Neurocritical Care. 2014;21(3):539-550\n'},{id:"B17",body:'\nTaylor T, Dineen RA, Gardiner DC, Buss CH, Howatson A, Pace NL. Computed tomography (CT) angiography for confirmation of the clinical diagnosis of brain death. Cochrane Database of Systematic Reviews. 2014;3:CD009694\n'},{id:"B18",body:'\nHopyan JJ, Gladstone DJ, Mallia G, Schiff J, Fox AJ, Symons SP, et al. Renal safety of CT angiography and perfusion imaging in the emergency evaluation of acute stroke. American Journal of Neuroradiology. 2008;29(10):1826-1830\n'},{id:"B19",body:'\nKrol AL, Dzialowski I, Roy J, Puetz V, Subramaniam S, Coutts SB, et al. Incidence of radiocontrast nephropathy in patients undergoing acute stroke computed tomography angiography. Stroke. 2007;38(8):2364-2366\n'},{id:"B20",body:'\nShankar JJS, Vandorpe R. CT perfusion for confirmation of brain death. American Journal of Neuroradiology. 2013;34(6):1175-1179\n'},{id:"B21",body:'\nShankar JJS, Woulfe J, Silva VD, Nguyen TB. Evaluation of perfusion CT in grading and prognostication of high-grade gliomas at diagnosis: A pilot study. American Journal of Roentgenology. 2013;200(5):W504-W509\n'},{id:"B22",body:'\nShankar JJS, Langlands G, Doucette S, Phillips S. CT perfusion in acute stroke predicts final infarct volume-inter-observer study. Canadian Journal of Neurological Sciences. 2016;43(1):93-97\n'},{id:"B23",body:'\nUwano I, Kudo K, Sasaki M, Christensen S, Østergaard L, Ogasawara K, et al. CT and MR perfusion can discriminate severe cerebral hypoperfusion from perfusion absence: Evaluation of different commercial software packages by using digital phantoms. Neuroradiology. 2012;54(5):467-474\n'},{id:"B24",body:'\nSawicki M, Sołek-Pastuszka J, Chamier-Ciemińska K, Walecka A, Bohatyrewicz R. Accuracy of computed tomographic perfusion in diagnosis of brain death: A prospective cohort study. Medical Science Monitor. 2018;24:2777-2785\n'},{id:"B25",body:'\nIshii K, Onuma T, Kinoshita T, Shiina G, Kameyama M, Shimosegawa Y. Brain death: MR and MR angiography. American Journal of Neuroradiology. 1996;17(4):731-735\n'},{id:"B26",body:'\nKarantanas AH, Hadjigeorgiou GM, Paterakis K, Sfiras D, Komnos A. Contribution of MRI and MR angiography in early diagnosis of brain death. European Radiology. 2002;12(11):2710-2716\n'},{id:"B27",body:'\nLövblad KO, Bassetti C, Basssetti C. Diffusion-weighted magnetic resonance imaging in brain death. Stroke. 2000;31(2):539-542\n'},{id:"B28",body:'\nDrake M, Bernard A, Hessel E. Brain death. The Surgical Clinics of North America. 2017;97(6):1255-1273\n'}],footnotes:[],contributors:[{corresp:null,contributorFullName:"Sudharsana Rao Ande",address:null,affiliation:'
Division of Neuroradiology, Department of Radiology, University of Manitoba, Winnipeg, MB, Canada
'},{corresp:"yes",contributorFullName:"Jai Jai Shiva Shankar",address:"shivajai1@gmail.com",affiliation:'
Division of Neuroradiology, Department of Radiology, University of Manitoba, Winnipeg, MB, Canada
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1. Introduction
Melatonin is a principal hormone produced by pineal cells in the pineal gland located in the cerebrum center behind the third ventricle (Figure 1). This endocrine gland consists of two cell types: pineal cells (which dominate and produce indolamines, mainly represented by melatonin, and peptides, such as arginine vasotocin) and neuroglia cells. The information received from neurons and modified by means of night and daylight intensity transforms in the pineal gland into chemical signals. Receiving the information about luminosity the pineal gland turns it into endocrine response by producing melatonin, which is a biogenic amine pertaining to the indole class, based on its chemical structure. Melatonin is a derivant of biogenic amine serotonin, which in its turn is synthesized from the amino acid tryptophan, received with food. Activity of ferments participating in serotonin transformation into melatonin is suppressed by lighting—that is why this hormone can be produced only during hours of darkness [1].
Figure 1.
Anatomical location for pineal body.
Key points
Melatonin functions in the human body are very diverse, and its normal secretion is extremely important for the preservation of somatic health.
The important role of melatonin in the formation of the reproductive function of women, the formation of a two-phase cycle, high-quality ovulation and fertilization, prevention of violations of a number of gynecological and obstetric pathologies.
Currently there are convincing data on the role of melatonin in the onset of menopause, the formation of climacteric syndrome, depression, osteoporosis, dyslipidemia, menopausal metabolic syndrome and cardiovascular diseases, and breast cancer in women in perimenopausal and postmenopausal women.
Melatonin is mainly released to the cerebrospinal fluid (liquor), getting from there to the blood flow and afterwards easily allocating itself in various organs and tissues due to good lipophilic properties [2]. Key effects of melatonin are connected with the action on membrane receptors—MT1 and MT2. They relate to a group of receptors connected with G-protein. These receptors are responsible for chronobiological effects and regulation of circadian rhythm and are widely distributed in different organs and tissues. Melatonin receptor presentation in the reproductive organs and receptors to sexual hormones in the epiphysis enables drawing the conclusion that melatonin plays an important role in regulation of reproductive aspect (Figure 2).
Figure 2.
Melatonin mechanisms of action.
In the same way, the nuclear receptors of melatonin ROR-α/RZR-β have been discovered. It is evident that many immune-stimulating and antitumoral effects are mediated by them.
Antioxidative function of melatonin is based on the receptor action, but this hormone is able to directly withdraw free radicals without receptor actuation [3].
Russian scientists discovered that apart from epiphyseal melatonin, there is an extrapineal one that is formed in different gastrointestinal tracts and other organs: liver, kidneys, supramental capsules, gall bladder, ovaries, endometrium, placenta, thymus, white blood cells, thrombocytes, and endothelium. Biologic action of the extrapineal melatonin is carried out right where it is synthesized [1].
2. Melatonin main physiological functions and its role in maintaining human health
During the recent years, new data on the mechanisms providing for the integral interaction among the nervous, immune, and endocrine systems have been received. Presumably, pineal gland is an integrator of such interaction, while its main hormone, melatonin, takes part in regulation of the activity of central and vegetative nervous systems, endocrine organs, and immune system. The performed investigations have demonstrated that melatonin fulfills an extremely wide range of physiological functions: biorhythmic and immunomodulatory processes, thermal control and sleep onset, and antioxidative and anti-stress effects [3]. Hormone secretion starts on the third month of infant development and reaches its peak during the first years (not later than at the age of 5). Before puberty, melatonin synthesis remains at a constantly high level [4]. During the age of 11–14, due to the fact that the pineal gland reduces melatonin production, the hormone mechanisms of sexual development are launched. The next significant reduction in activity occurs simultaneously with menopause onset—at the age of 45–60. With the aging progression, along with decrease in basal level, melatonin secretion peaks are getting lower [1]. During daytime melatonin concentration in the blood serum remains low (10–20 pg/ml), while during the night hours it grows considerably (80,120 pg/ml) and reaches its maximum value between midnight and 3–5 a.m. Melatonin secretion usually starts at 9 p.m. and terminates at 7–9 a.m. Melatonin metabolites are found in urine: 6-sulfatoxymelatonin (80–90%) and 6-hydroxyglucuronide (10–20%) corresponding to the circadian rhythm that is very close to the rhythm of melatonin secretion [5].
A new science, biorhythmology, introduced the notion of desynchronosis—clinically very important—that means ill-being or pathological syndrome, which is connected with the unbalance of circadian rhythms. A degree of desynchronosis is defined by the quantity and rhythm of melatonin production during the day and night. It has been determined that when a somatic disease goes hard or aggravates, melatonin production is getting worse, and its night indicator is getting closer to the day value [6]. Disturbed melatonin secretion finds its clinical manifestation in tiredness, indisposition, sleep disorder, and sometimes aggravation of a chronic disease or even appearance of a new one. Desynchronosis condition is exemplified by jet lag syndrome caused by rapid long-distance transmeridian travel [7].
It is generally known that melatonin has an antidepressant function. However, foreign colleagues stated disturbed circadian rhythm of melatonin secretion experienced by patients with depression during a menopause along with its increase during the morning hours as compared with women in good health that also has impact on sleep, level of follicle-stimulating hormone, and body mass index [8]. A connection was established between sleep disorder and melatonin reduction in female saliva during perimenopause without registering such pattern among women in postmenopause [9].
Therefore, melatonin functions in a human body are quite diversified, and its normal secretion is highly important for maintaining human health in a contemporary world.
3. Melatonin involvement into hormonal regulation of female reproductive system functions and its aging
In 1963 R.J. Wurtman et al. reported for the first time that exogenic intake of melatonin causes weight reduction in female rat ovaries. Since those times many evidences that pineal gland and its main hormone, melatonin, influence reproductive function have been received. Studies showed that neurons in preoptic and mediobasal areas of hypothalamus and hypophysis represented the main points, through which melatonin produced its reproductive action. The main physiological effect of melatonin lies in the slowdown of gonadotrophin secretion, with greater suppression of the lutenizing hormone (LH) by melatonin rather than the follicle-stimulating one. Negative correlation is registered between melatonin level at night and lutenizing hormone concentration. In addition, secretion of other tropic hormones of hypophysis anterior lobe (such as corticotrophin, thyrotropin, somatotropin) is reduced, though to a lesser extent. Melatonin can be called a universal inhibitor of endocrine function in a female body [10].
Melatonin takes part in regulation of many vital physiological processes, such as puberty and genital formation, menstrual cycle, and aging of reproductive system. High level of nocturnal melatonin was found in children with delayed puberty, while among children having accelerated puberty, a decrease in melatonin secretion at night was noted. High levels of melatonin among children produce a dominating effect on pulsatile gonadotropin secretion, ovary function, and puberty [4].
Abnormal levels of melatonin in blood are connected with a number of malfunctions in the system “hypothalamus—hypophysis—ovaries.” This gives boost to precocious puberty or its delay and formation of hypothalamic or hypergonadotropic amenorrhea. Therefore, melatonin may have indirect influence on the function of reproductive glands through its intervention into the secretion of gonadotropin-releasing hormone and/or secretion of gonadotrophins. Some data demonstrate that melatonin can also be synthesized in reproductive glands. Decreased melatonin secretion in summer coincides with higher fertility among women living in the Northern Hemisphere [11].
Based on these data, it was presupposed that melatonin could be a part of events preceding activation of hypothalamus-ovary axis during a puberty period [12]. Non-serial MRI of female head region helped register a reliable decrease in pineal gland volume during the ovulatory phase as well as while perimenopause. It indicates pineal gland involvement into “turning off” female reproductive function [13].
Melatonin may also produce direct influence on ovaries. High level of melatonin was found in preovulatory follicular fluid with triple concentration as compared to blood. Connecting areas of iodine melatonin were identified in human cells of granulosis and preovulatory follicles.
Antioxidative effect of melatonin is considered to be the most prominent one. It has been determined that melatonin ties free radicals of oxygen and at the same time stimulates enzymatic systems and SOD and possesses protective properties in relation to free-radical damage of DNA [14].
It’s generally known that macrofags, neutrophils, and vascular endothelium cells located in follicles produce AOS during ovulation. Despite the fact that AOS (active oxygen species) participate in breaking follicles, potentially they may damage an ovum and granulosis lutein cells. AOS inhibit progesterone production by lutein cells due to inhibition of steroidogenesis enzymes and transport intracellular protein. Melatonin is an important antioxidant in ovary follicles and enables progesterone synthesis by luteal cells [15]. Research outcomes have shown that melatonin intake leads to increased concentration of this hormone in follicular fluid and reduced oxidative damage inside follicles, thus raising a chance of fertilization and pregnancy [16, 17]. Melatonin intake also improved progesterone synthesis among women with infertility issues caused by insufficiency of the cycle luteal phase [18].
Pregnancy and acts of delivery are characterized by deep alterations in the endocrine profile of a female body as well as in pineal gland operation. In the case of physiological pregnancy, increased melatonin excretion with urine is marked, while just before an act of delivery its level plummets.
Decreased melatonin level is noted in the case of threatening miscarriage [4].
At the same time, many scientists speak about the great importance of melatonin in the body aging process. It is also pointed out that from the age of 45, melatonin starts to decline steadily till the end of human life. Numerous studies have demonstrated the correlation between melatonin synthesis and menopause onset [19]. The second decrease in melatonin level may be related to involutory processes in pineal gland [13].
In a placebo-controlled clinical study, it was established that there was a connection between decreased content of nocturnal melatonin in saliva and menopause onset, while intake of 3 mg of melatonin by female patients during perimenopause on a daily basis for 6 months eliminates hormonal and neurovegetative disorders and recovers menstruation cycle and thyroid function [20].
Women in postmenopause had lower concentration of melatonin in blood serum as compared to women in perimenopause, with a shorter duration of melatonin secretion in postmenopause as a rule, while melatonin synthesis peak time (acrophase) was almost the same. A pattern was determined that as melatonin secretion peak occurs later among women in perimenopause, anxiety level gets higher (p = 0.022), and as melatonin secretion continues for a longer period, the quality of life among patients gets better (p < 0.001) [21].
Some scientists suggest using melatonin drugs at the first stage of climacteric disorder treatment even before the start of hormonal therapy of menopause [4]. Moreover, in a double-blind placebo-controlled clinical study, it was determined that prescription of menopause hormonal therapy to postmenopausal women shifts melatonin secretion peak time without changing the melatonin level in the blood serum, which requires further research [21]. Other authors did not found in their research analyses devoted to alternative therapy for climacteric disorders any convincing data on hot flash arresting by melatonin drug [22].
4. Melatonin lipid metabolism
A growing number of evidences are emerging, which point to melatonin involvement into lipid metabolism. The study of H. Tamura was devoted to melatonin influence on lipid metabolism among women in perimenopause and postmenopause. A negative correlation was established between nocturnal melatonin and total cholesterol level, low-density lipoprotein, and positive correlation with high-density lipoprotein. No correlation was found between nocturnal melatonin and triglyceride level in blood. These findings show that melatonin drug prescription may represent a new approach to the correction of lipid metabolism and prevention of cardiovascular diseases during perimenopause and postmenopause [23]. Other scientists determined that melatonin improves lipid profile (leads to a reduced level of low-density lipoprotein) and fulfills antioxidant protection [24].
Under a study led by L.I. Maltseva [25], scientists analyzed melatonin role in the development of climacteric syndrome and its effectiveness for treating pathological climacterium. Russian scientists established that the level of 6-sulfatoxymelatonin in a 24-h urine among patients with severe climacteric syndrome amounts to 35.09 ± 3.5 ng/ml, medium severity (44.01 ± 7.92 ng/ml), and mild climacteric syndrome (45.91 ± 12.42 ng/ml) (1.7 times lower as compared to women in good health). Accordingly, secretory function of hypophysis is altered in various ways. Women with low level of 6-sulfatoxymelatonin in a 24-h urine show significant growth of both gonadotropic hormones—follicle-stimulating and luteinizing hormones—in a proportional way. A research showed that women had a high level of catecholamines (adrenaline and noradrenaline) with its degree being dependent on climacteric syndrome severity. It was also determined that women in perimenopausal age have increased the level of atherogenic fractions of blood lipids on the background of lower melatonin level.
Scientists came to the conclusion that melatonin acts as a modifier of alterations which occur with the development of climacteric disorders and influence hormonal, mediating, and biochemical indicators of the female body. Women with mild climacteric syndrome taking 3 mg of melatonin per day as monotherapy demonstrated during the repeated evaluation of clinical, hormonal, and biochemical indicators after 1 month a positive dynamics of all indicators. The blood hormone level was close to reference values, follicle-stimulating hormone level dropped by 2.29 times, luteinizing hormone level by 2.1 times. Values of melatonin sulfate in a 24-h urine grew by 2.64 times and were close as never to the reference values 27.95 ± 7.92…73.95 ± 24.85 ng/ml. However more significant alterations were noted for the severe climacteric syndrome without any side effects when melatonin treatment and menopause hormonal therapy were used together [25].
5. Menopause and sleep disturbance
Japanese scientists stated that estradiol level was firmly higher among women that worked night shifts and went to sleep later than 1 a.m. as compared to women that slept at night, with the level of serum testosterone and DHEA-sulfate unaffected, while 6-sulfatoxymelatonin concentration in urine was lower among the first group patients. Similar hormonal disruptions among postmenopausal women experiencing sleep disorder represent serious risk factors of breast cancer [26]. Singapore Chinese Health Study (2008) also showed that among women in postmenopause, the risk of breast cancer gets lower when sleep duration increases (p = 0.047). When sleep duration exceeds 9 h, a relative risk equals to 0.67 (95% confidence interval 0.4–1.1) as compared to women with a sleep duration of 6 h or less. At that, melatonin level was higher by 42% when sleep duration was 9 h or more. Such pattern was registered for women with normal weight (body mass index of 23.2 kg/m), p = 0.024 [27]. American scientists proved through a largescale prospective analysis that among women with 6-sulfatoxymelatonin content within the upper quartile, there were fewer with invasive breast cancer than among those whose values were within the bottom quartile [28]. It was established that the increased concentration of 6-sulfatoxymelatonin in the morning urine portion was statistically related to a lower risk of breast cancer (ratio of chances for upper and lower quartiles of 6-sulfatoxymelatonin level 0.62; 95% confidence interval 0.41–0.95; p = 0.004) [29].
C.G. Harrod and his colleagues made an assumption that a growing risk of cerebrovascular disease registered among menopausal women can be to some extent explained by changes in the level of circulating melatonin and estrogens and their modulating influence on biologic activity of endothelial cells, including vascular tone regulation, leukocytes adhesion, and angiogenesis. This hypothesis is confirmed by numerous studies demonstrating the braking effect of melatonin and estrogens on vessel tone, neuroprotection, and expression of receptors [30].
Increased melatonin secretion in the morning is more typical for menopausal patients with depression than women in good health. Moreover, menopause duration, level of the follicle-stimulating hormone, sleep end time, and body mass index may lead to alterations in melatonin secretion when suffering from depression during a menopause [8].
6. Melatonin effects on bone metabolism
At present a relation between melatonin and skeleton is known. Melatonin may produce an effect on bone tissue which manifests itself in bone tissue formation with osteoblasts and/or hindering bone resorption with osteoclasts. The study of K. Satomura et al. [31] confirms the melatonin (Mel1) receptor expression in human osteoblasts and tendency of its level reduction with aging. It is also demonstrated that melatonin can have a boosting effect on proliferation and differentiation of human osteoblasts [32]. Through a controlled randomized trial (2012), exogenous melatonin effect on bone tissue density was revealed. Bone tissue condition was controlled in two ways—bone tissue density estimation and bone marker determination. There was no considerable improvement noted in terms of bone tissue density in T points or as compared with placebo. An average change in the activity of bone resorption marker, N-telopeptide (NTX), in this study did not differ much inside and between the groups. Similarly, the average change in the activity of bone formation marker, osteocalcin, did not show any remarkable differences either inside a group or between groups. However, NTX to osteocalcin ratio followed a downward trend among the women who took melatonin as compared to placebo. It is quite important because among menopausal women, this ratio is known to increase so that osteoclasts activity outstrips osteoblast activity, which leads to a loss of bone mass. Probably, decreased level of nocturnal melatonin that occurs during a menopause causes hormonal unbalance and perimenopause symptoms, including the loss in bone mass. These data prove that melatonin intake may enable the balancing of bone resorption and formation processes, potentially preventing fast loss of bone mass attributed to a menopausal period [33].
Melatonin inhibits resorption activity by reducing RANKL-mediated osteoclastogenesis and therefore decreases bone resorption. Melatonin also protects from losing bone mass induced by free radicals, which occurs in the case of extreme bone resorption, due to its powerful antioxidative properties [34, 35]. In addition to its direct effect on the bone tissue, melatonin can produce an indirect influence on bone metabolism through the hypothalamus-pituitary axis, by suppressing levels of follicle-stimulating hormone and estrogen and increasing the level of progesterone. In contrast to the follicle-stimulating hormone, melatonin has positive correlation with progesterone level. Progesterone is known to influence on the mineral density of bone tissue, especially on osteoblast differentiation [36]. Reduced level of progesterone during a perimenopause may lead to the decreasing of bone tissue density because of osteoblasts loss.
7. Conclusion
Therefore, melatonin role in a female body is quite significant from the moment of birth till the last breath. It is revealed that up to the present time according to the literature data there is no information about the standards of secretion of melatonin for women of different age groups, and the lack of secretion of melatonin can be judged by clinical manifestations, and also when compared with groups of healthy women. The issues of using melatonin treatment for different cases of pregnancy complications and gynecological disorders remain unclear. Long-term intake of melatonin to treat pathological menopause is still to be discussed.
\n',keywords:"women, pineal gland, melatonin, 6-sulfatoxymelatonin",chapterPDFUrl:"https://cdn.intechopen.com/pdfs/70178.pdf",chapterXML:"https://mts.intechopen.com/source/xml/70178.xml",downloadPdfUrl:"/chapter/pdf-download/70178",previewPdfUrl:"/chapter/pdf-preview/70178",totalDownloads:214,totalViews:0,totalCrossrefCites:0,dateSubmitted:"May 7th 2019",dateReviewed:"August 2nd 2019",datePrePublished:"November 23rd 2019",datePublished:null,dateFinished:null,readingETA:"0",abstract:"In the presented article, we cover the issues concerning physiology of secretion of pineal hormone melatonin and its role in the vital processes of a body. Focus is given to melatonin effect on the female reproductive system, its participation in the aging process, and formation of pathological menopause. The article also presents research data on the effectiveness of the melatonin drug when tackling climacteric syndrome. It is revealed that according to the available literature up to date there is no information about the standards of secretion of melatonin for women of different age groups, and the lack of secretion of melatonin can be judged by clinical manifestations and also when compared with groups of healthy women. The issues of the melatonin drug application at various complications of pregnancy and gynecological diseases remain unclear. Long-term intake of melatonin to treat pathologic menopause is still to be discussed.",reviewType:"peer-reviewed",bibtexUrl:"/chapter/bibtex/70178",risUrl:"/chapter/ris/70178",signatures:"Elena N. Usoltseva and Marina V. Danilova",book:{id:"7980",title:"Hormone Therapy and Replacement in Cancer and Aging-related Diseases",subtitle:null,fullTitle:"Hormone Therapy and Replacement in Cancer and Aging-related Diseases",slug:"hormone-therapy-and-replacement-in-cancer-and-aging-related-diseases",publishedDate:"July 22nd 2020",bookSignature:"Leticia B. A. Rangel, Hephzibah Kirubamani, Ian Victor Silva and Paulo Cilas Morais Lyra Junior",coverURL:"https://cdn.intechopen.com/books/images_new/7980.jpg",licenceType:"CC BY 3.0",editedByType:"Edited by",editors:[{id:"60359",title:"Dr.",name:"Letícia",middleName:null,surname:"Rangel",slug:"leticia-rangel",fullName:"Letícia Rangel"}],productType:{id:"1",title:"Edited Volume",chapterContentType:"chapter",authoredCaption:"Edited by"}},authors:null,sections:[{id:"sec_1",title:"1. Introduction",level:"1"},{id:"sec_2",title:"2. Melatonin main physiological functions and its role in maintaining human health",level:"1"},{id:"sec_3",title:"3. Melatonin involvement into hormonal regulation of female reproductive system functions and its aging",level:"1"},{id:"sec_4",title:"4. Melatonin lipid metabolism",level:"1"},{id:"sec_5",title:"5. Menopause and sleep disturbance",level:"1"},{id:"sec_6",title:"6. Melatonin effects on bone metabolism",level:"1"},{id:"sec_7",title:"7. 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Journal of the American Pharmacists Association. 2010;50(5):106-115'},{id:"B23",body:'Tamura H, Nakamura Y, Narimatsu A, et al. Melatonin treatment in peri- and postmenopausal women elevates serum high-density lipoprotein cholesterol levels without influencing total cholesterol levels. Journal of Pineal Research. 2008;45:101-105'},{id:"B24",body:'Kozirog M, Poliwczak AR, Duchnowicz P, et al. Melatonin treatment improves blood pressure, lipid profile, and parameters of oxidative stress in patients with metabolic syndrome. Journal of Pineal Research. 2011;50:261-266'},{id:"B25",body:'Maltseva LI, Gafarova EA, Garipova GH. Melatonin role in reproductive glands function regulation and possibility of its use for pathological climacteric symptoms treatment. Advances in Gerontology. 2007;4(20):68-74'},{id:"B26",body:'Nagata C, Nagao Y, Yamamoto S, et al. Light exposure at night, urinary 6sulfatoxymelatonin, and serum estrogens and androgens in postmenopausal Japanese women. Cancer Epidemiology, Biomarkers & Prevention. 2008;17(6):1418-1423'},{id:"B27",body:'Wu AH, Wang R, Koh WP. et al, Sleep duration, melatonin and breast cancer among Chinese women in Singapore. Carcinogenesis. 2008;29(6):1244-1248'},{id:"B28",body:'Schernhammer ES, Berrino F, Krogh V, et al. Urinary 6-sulfatoxymelatonin levels and risk of breast cancer in post-menopausal women. Journal of the National Cancer Institute. 2008;100(12):898-905'},{id:"B29",body:'Schernhammer ES, Hankinson SE. Urinary melatonin levels and postmenopausal breast cancer risk in the nurses’ health study cohort. Cancer Epidemiology, Biomarkers & Prevention. 2009;18(1):74-79'},{id:"B30",body:'Harrod CG, Bendok BR, Hunt Batjer H. Interactions between mela tonin and estrogen may regulate cerebrovascular function in women: Clinical implications for the effective use of HRT during menopause and aging. Medical Hypotheses. 2008;70(1):213'},{id:"B31",body:'Satomura K, Tobiume S, Tokuyama R, Yamasaki Y, et al. Melatonin at pharmacological doses enhances human osteoblastic differentiation in vitro and promotes mouse cortical bone formation in vivo. Journal of Pineal Research. 2007 Apr;42(3):231-239'},{id:"B32",body:'Park KH, Kang JW, Lee EM, et al. Melatonin promotes osteoblastic differentiation through the BMP/ERK/Wnt signaling pathways. Journal of Pineal Research. 2011;51:187-194'},{id:"B33",body:'Kotlarczyk MP, Lassila HC, O’Neil CK, et al. Melatonin osteoporosis prevention study (MOPS): A randomized, double-blind, placebo-controlled study examining the effects of melatonin on bone health and quality of life in perimenopausal women. Journal of Pineal Research. 2012;52(4):414-426'},{id:"B34",body:'Galano A, Tan DX, Reiter RJ. Melatonin as a natural ally against oxidative stress: A physicochemical examination. Journal of Pineal Research. 2011;51:1-16'},{id:"B35",body:'Sanchez-Barcelo EJ, Mediavilla MD, Tan DX, et al. 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The Open Access model is applied to all of our publications and is designed to eliminate subscriptions and pay-per-view fees. This approach ensures free, immediate access to full text versions of your research.
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For Authors who are still unable to obtain funding from their institutions or research funding bodies for individual projects, IntechOpen does offer the possibility of applying for a Waiver to offset some or all processing feed. Details regarding our Waiver Policy can be found here.
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