Critical infrastructure sectors in US-NIPP and EU 114/08.
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These books synthesize perspectives of renowned scientists from the world’s most prestigious institutions - from Fukushima Renewable Energy Institute in Japan to Stanford University in the United States, including Columbia University (US), University of Sidney (AU), University of Miami (USA), Cardiff University (UK), and many others.
\\n\\nThis collaboration embodied the true essence of Open Access by simplifying the approach to OA publishing for Academic editors and authors who contributed their research and allowed the new research to be made available free and open to anyone anywhere in the world.
\\n\\nTo celebrate the 50 books published, we have gathered them at one location - just one click away, so that you can easily browse the subjects of your interest, download the content directly, share it or read online.
\\n\\n\\n\\n\\n"}]',published:!0,mainMedia:null},components:[{type:"htmlEditorComponent",content:'
IntechOpen and Knowledge Unlatched formed a partnership to support researchers working in engineering sciences by enabling an easier approach to publishing Open Access content. Using the Knowledge Unlatched crowdfunding model to raise the publishing costs through libraries around the world, Open Access Publishing Fee (OAPF) was not required from the authors.
\n\nInitially, the partnership supported engineering research, but it soon grew to include physical and life sciences, attracting more researchers to the advantages of Open Access publishing.
\n\n\n\nThese books synthesize perspectives of renowned scientists from the world’s most prestigious institutions - from Fukushima Renewable Energy Institute in Japan to Stanford University in the United States, including Columbia University (US), University of Sidney (AU), University of Miami (USA), Cardiff University (UK), and many others.
\n\nThis collaboration embodied the true essence of Open Access by simplifying the approach to OA publishing for Academic editors and authors who contributed their research and allowed the new research to be made available free and open to anyone anywhere in the world.
\n\nTo celebrate the 50 books published, we have gathered them at one location - just one click away, so that you can easily browse the subjects of your interest, download the content directly, share it or read online.
\n\n\n\n\n'}],latestNews:[{slug:"webinar-introduction-to-open-science-wednesday-18-may-1-pm-cest-20220518",title:"Webinar: Introduction to Open Science | Wednesday 18 May, 1 PM CEST"},{slug:"step-in-the-right-direction-intechopen-launches-a-portfolio-of-open-science-journals-20220414",title:"Step in the Right Direction: IntechOpen Launches a Portfolio of Open Science Journals"},{slug:"let-s-meet-at-london-book-fair-5-7-april-2022-olympia-london-20220321",title:"Let’s meet at London Book Fair, 5-7 April 2022, Olympia London"},{slug:"50-books-published-as-part-of-intechopen-and-knowledge-unlatched-ku-collaboration-20220316",title:"50 Books published as part of IntechOpen and Knowledge Unlatched (KU) Collaboration"},{slug:"intechopen-joins-the-united-nations-sustainable-development-goals-publishers-compact-20221702",title:"IntechOpen joins the United Nations Sustainable Development Goals Publishers Compact"},{slug:"intechopen-signs-exclusive-representation-agreement-with-lsr-libros-servicios-y-representaciones-s-a-de-c-v-20211123",title:"IntechOpen Signs Exclusive Representation Agreement with LSR Libros Servicios y Representaciones S.A. de C.V"},{slug:"intechopen-expands-partnership-with-research4life-20211110",title:"IntechOpen Expands Partnership with Research4Life"},{slug:"introducing-intechopen-book-series-a-new-publishing-format-for-oa-books-20210915",title:"Introducing IntechOpen Book Series - A New Publishing Format for OA Books"}]},book:{item:{type:"book",id:"8091",leadTitle:null,fullTitle:"Autonomic Nervous System Monitoring - Heart Rate Variability",title:"Autonomic Nervous System Monitoring",subtitle:"Heart Rate Variability",reviewType:"peer-reviewed",abstract:"Heart rate variability (HRV) is considered a reliable reflection of the many physiological factors modulating the normal rhythm of the heart. It reflects autonomic nervous system (ANS) function, and as such, it is used in numerous fields of medicine. Written by experts in the field, this book provides a comprehensive overview of HRV. The first section is dedicated to technical themes related to monitoring and the variables recorded. The second section highlights use of HRV in hypothermia. Finally, the third section covers general aspects of HRV application.",isbn:"978-1-83880-519-7",printIsbn:"978-1-83880-518-0",pdfIsbn:"978-1-83880-577-7",doi:"10.5772/intechopen.77922",price:119,priceEur:129,priceUsd:155,slug:"autonomic-nervous-system-monitoring-heart-rate-variability",numberOfPages:138,isOpenForSubmission:!1,isInWos:1,isInBkci:!1,hash:"98067dd53efd76b17cf31d1664f88982",bookSignature:"Theodoros Aslanidis",publishedDate:"May 20th 2020",coverURL:"https://cdn.intechopen.com/books/images_new/8091.jpg",numberOfDownloads:6460,numberOfWosCitations:2,numberOfCrossrefCitations:7,numberOfCrossrefCitationsByBook:0,numberOfDimensionsCitations:14,numberOfDimensionsCitationsByBook:0,hasAltmetrics:0,numberOfTotalCitations:23,isAvailableForWebshopOrdering:!0,dateEndFirstStepPublish:"April 30th 2019",dateEndSecondStepPublish:"September 19th 2019",dateEndThirdStepPublish:"November 18th 2019",dateEndFourthStepPublish:"February 6th 2020",dateEndFifthStepPublish:"April 6th 2020",currentStepOfPublishingProcess:5,indexedIn:"1,2,3,4,5,6",editedByType:"Edited by",kuFlag:!1,featuredMarkup:null,editors:[{id:"200252",title:"Dr.",name:"Theodoros",middleName:null,surname:"Aslanidis",slug:"theodoros-aslanidis",fullName:"Theodoros Aslanidis",profilePictureURL:"https://mts.intechopen.com/storage/users/200252/images/system/200252.png",biography:"Dr. Theodoros K. Aslanidis received an MD from Plovdiv Medical University, Bulgaria, and a Ph.D. from Aristotle University of Thessaloniki, Greece. After serving as a medical doctor in the Hellenic Army Force and as a rural physician at Outhealth Centre, Iraklia and Serres’ General Hospital, Greece, he completed anesthesiology specialty training at Hippokratio General Hospital of Thessaloniki. He also completed Critical Care subspecialty training at AHEPA University Hospital, and the Prehospital Emergency Medicine postgraduate program, Hellenic National Centre for Emergency Care. He served as an EMS physician and emergency communication center medic before moving to his current post as consultant-researcher at the Intensive Care Unit, St. Paul General Hospital of Thessaloniki, Greece. He also serves as a senior lecturer in the Research Faculty, College of Offshore and Remote Medicine, Pretty Bay, Malta.",institutionString:"Saint Paul General Hospital of Thessaloniki",position:null,outsideEditionCount:0,totalCites:0,totalAuthoredChapters:"3",totalChapterViews:"0",totalEditedBooks:"5",institution:null}],equalEditorOne:null,equalEditorTwo:null,equalEditorThree:null,coeditorOne:null,coeditorTwo:null,coeditorThree:null,coeditorFour:null,coeditorFive:null,topics:[{id:"983",title:"Cardiac Electrophysiology",slug:"cardiac-electrophysiology"}],chapters:[{id:"69051",title:"HRV in an Integrated Hardware/Software System Using Artificial Intelligence to Provide Assessment, Intervention and Performance Optimization",doi:"10.5772/intechopen.89042",slug:"hrv-in-an-integrated-hardware-software-system-using-artificial-intelligence-to-provide-assessment-in",totalDownloads:739,totalCrossrefCites:2,totalDimensionsCites:2,hasAltmetrics:0,abstract:"Heart rate variability (HRV) is increasingly recognized as a central variable of interest in health maintenance, disease prevention and performance optimization. It is also a sensitive biomarker of health status, disease presence and functional abilities, acquiring and processing high fidelity inter beat interval data, along with other psychophysiological parameters that can assist in clinical assessment and intervention, population health studies/digital epidemiology and positive performance optimization. We describe a system using high-throughput artificial intelligence based on the KUBIOS platform to combine time, frequency and nonlinear data domains acquired by wearable or implanted biosensors to guide in clinical assessment, decision support and intervention, population health monitoring and individual self-regulation and performance enhancement, including the use of HRV biofeedback. This approach follows the iP4 health model which emphasizes an integral, personalized, predictive, preventive and participatory approach to human health and well-being. It therefore includes psychological, biological, genomic, sociocultural, evolutionary and spiritual variables as mutually interactive elements in embodying complex systems adaptation.",signatures:"Robert L. Drury",downloadPdfUrl:"/chapter/pdf-download/69051",previewPdfUrl:"/chapter/pdf-preview/69051",authors:[{id:"305353",title:"Dr.",name:"Robert",surname:"Drury",slug:"robert-drury",fullName:"Robert Drury"}],corrections:null},{id:"71001",title:"Root Mean Square of the Successive Differences as Marker of the Parasympathetic System and Difference in the Outcome after ANS Stimulation",doi:"10.5772/intechopen.89827",slug:"root-mean-square-of-the-successive-differences-as-marker-of-the-parasympathetic-system-and-differenc",totalDownloads:927,totalCrossrefCites:3,totalDimensionsCites:4,hasAltmetrics:0,abstract:"The autonomic nervous system has a huge impact on the cardiac regulatory mechanism, and many markers exist for evaluating it. In this chapter we are going to focus on the RMSSD (Root mean square of successive differences), considered the most precise marker for the parasympathetic effector on the heart. Before is necessary to learn what the Heart Rate Variability is and how it works, which type of range of HRV exists and how we can measure it. Finally, there will be a presentation of how the RMSSD can be used in different field, and how and why the outcome can change and what does it mean.",signatures:"Giovanni Minarini",downloadPdfUrl:"/chapter/pdf-download/71001",previewPdfUrl:"/chapter/pdf-preview/71001",authors:[{id:"307733",title:"M.Sc.",name:"Giovanni",surname:"Minarini",slug:"giovanni-minarini",fullName:"Giovanni Minarini"}],corrections:null},{id:"70280",title:"Heart Rate Variability Recording System Using Photoplethysmography Sensor",doi:"10.5772/intechopen.89901",slug:"heart-rate-variability-recording-system-using-photoplethysmography-sensor",totalDownloads:884,totalCrossrefCites:2,totalDimensionsCites:5,hasAltmetrics:0,abstract:"Heart rate variability (HRV) is a physiological measurement that can help to monitor and diagnose chronic diseases such as cardiovascular disease, depression, and psychological stress. HRV measurement is commonly extracted from the electrocardiography (ECG). However, ECG has bulky wires where it needs at least three surface electrodes to be placed on the skin. This may cause distraction during the recording and need longer time to setup. Therefore, photoplethysmography (PPG), a simple optical technique, was suggested to obtain heart rate. This study proposes to investigate the effectiveness of PPG recording and derivation of HRV for feature analysis. The PPG signal was preprocessed to remove all the noise and to extract the HRV. HRV features were collected using time-domain analysis (TA), frequency-domain analysis (FA) and nonlinear time-frequency analysis (TFA). Five out of 22 HRV features, which are HR, RMSSD, LF/HF, LFnu, and HFnu, showed high correlation (rho > 0.6 and prho < 0.05) in comparison to standard 5-min excerpt while producing significant difference (p-value < 0.05) during the stressing condition across all interval HRV excerpts. This simple yet accurate PPG recording system perhaps might useful to assess the HRV signal in a short time, and further can be used for the ANS assessment.",signatures:"Noor Aimie-Salleh, Nurul Aliaa Abdul Ghani, Nurhafiezah Hasanudin and Siti Nur Shakiroh Shafie",downloadPdfUrl:"/chapter/pdf-download/70280",previewPdfUrl:"/chapter/pdf-preview/70280",authors:[{id:"307771",title:"Dr.",name:"Noor",surname:"Aimie-Salleh",slug:"noor-aimie-salleh",fullName:"Noor Aimie-Salleh"},{id:"308225",title:"Ms.",name:"Nurhafiezah",surname:"Hasanudin",slug:"nurhafiezah-hasanudin",fullName:"Nurhafiezah Hasanudin"},{id:"312328",title:"Ms.",name:"Siti Nur",surname:"Shakiroh",slug:"siti-nur-shakiroh",fullName:"Siti Nur Shakiroh"},{id:"312329",title:"Ms.",name:"Nurul Aliaa",surname:"Abdul Ghani",slug:"nurul-aliaa-abdul-ghani",fullName:"Nurul Aliaa Abdul Ghani"}],corrections:null},{id:"63852",title:"Modeling Thermoregulatory Responses to Cold Environments",doi:"10.5772/intechopen.81238",slug:"modeling-thermoregulatory-responses-to-cold-environments",totalDownloads:1140,totalCrossrefCites:0,totalDimensionsCites:1,hasAltmetrics:0,abstract:"The ability to model and simulate the rise and fall of core body temperature is of significant interest to a broad spectrum of organizations. These organizations include the military, as well as both public and private health and medical groups. To effectively use cold models, it is useful to understand the first principles of heat transfer within a given environment as well as have an understanding of the underlying physiology, including the thermoregulatory responses to various conditions and activities. The combination of both rational or first principles and empirical approaches to modeling allow for the development of practical models that can predict and simulate core body temperature changes for a given individual and ultimately provide protection from injury or death. The ability to predict these maximal potentials within complex and extreme environments is difficult. The present work outlines biomedical modeling techniques to simulate and predict cold-related injuries, and discusses current and legacy models and methods.",signatures:"Adam W. Potter, David P. Looney, Xiaojiang Xu, William R. Santee and Shankar Srinivasan",downloadPdfUrl:"/chapter/pdf-download/63852",previewPdfUrl:"/chapter/pdf-preview/63852",authors:[{id:"262568",title:"Mr.",name:"Adam",surname:"Potter",slug:"adam-potter",fullName:"Adam Potter"},{id:"271096",title:"Dr.",name:"David",surname:"Looney",slug:"david-looney",fullName:"David Looney"},{id:"271097",title:"Dr.",name:"Xiaojiang",surname:"Xu",slug:"xiaojiang-xu",fullName:"Xiaojiang Xu"},{id:"271098",title:"Dr.",name:"William",surname:"Santee",slug:"william-santee",fullName:"William Santee"},{id:"271099",title:"Prof.",name:"Shankar",surname:"Srinivasan",slug:"shankar-srinivasan",fullName:"Shankar Srinivasan"}],corrections:null},{id:"63545",title:"Techniques to Reduce the Magnitude and Duration of Redistribution Hypothermia in Adults",doi:"10.5772/intechopen.80830",slug:"techniques-to-reduce-the-magnitude-and-duration-of-redistribution-hypothermia-in-adults",totalDownloads:547,totalCrossrefCites:0,totalDimensionsCites:0,hasAltmetrics:0,abstract:"While much effort has been devoted to correcting intraoperative hypothermia and documenting the adverse outcomes associated with hypothermia, less attention has been directed to preventing redistribution hypothermia in the first place. Methods currently exist that can reduce the magnitude of redistribution hypothermia, but are not widely practiced. This chapter focuses on the pathophysiology of redistribution hypothermia and the currently available methods that can be employed to reduce redistribution hypothermia. Additional promising, but currently unproven, methods are discussed. Since hypothermia causes adverse outcomes, it is anticipated that the reduction in redistribution hypothermia will improve patient outcome.",signatures:"Jonathan V. Roth",downloadPdfUrl:"/chapter/pdf-download/63545",previewPdfUrl:"/chapter/pdf-preview/63545",authors:[{id:"267272",title:"Dr.",name:"Jonathan V",surname:"Roth",slug:"jonathan-v-roth",fullName:"Jonathan V Roth"}],corrections:null},{id:"68750",title:"Heart Rate Variability as Biomarker for Prognostic of Metabolic Disease",doi:"10.5772/intechopen.88766",slug:"heart-rate-variability-as-biomarker-for-prognostic-of-metabolic-disease",totalDownloads:745,totalCrossrefCites:0,totalDimensionsCites:0,hasAltmetrics:0,abstract:"Lifestyle emerging diseases like obesity, metabolic syndrome (MeS), and diabetes mellitus are considered high-risk factors for lethal arrhythmias and side effects. A Poincaré plot is constructed with the time series of RR and PP electrocardiogram (ECG) intervals, using two stages: the new phase and the old phase. We proposed this diagram of two dimensions, a way to quantify and observe the regularity of events in space and time. Therefore, the heart rate variability (HRV) can be used as a biomarker for early prognostic and diagnostic of several metabolic diseases; additionally, this biomarker is obtained by a noninvasive tool like the electrocardiogram.",signatures:"Alondra Albarado-Ibañez, Rosa Elena Arroyo-Carmona, Daniela Alexandra Bernabé-Sánchez, Marissa Limón-Cantú, Benjamín López-Silva, Martha Lucía Ita-Amador and Julián Torres-Jácome",downloadPdfUrl:"/chapter/pdf-download/68750",previewPdfUrl:"/chapter/pdf-preview/68750",authors:[{id:"305458",title:"Ph.D.",name:"Julian",surname:"Torres-Jacome",slug:"julian-torres-jacome",fullName:"Julian Torres-Jacome"},{id:"305461",title:"Dr.",name:"Alondra",surname:"Albardo-Ibañez",slug:"alondra-albardo-ibanez",fullName:"Alondra Albardo-Ibañez"},{id:"305462",title:"Dr.",name:"Rosa Elena",surname:"Arroyo-Carmona",slug:"rosa-elena-arroyo-carmona",fullName:"Rosa Elena Arroyo-Carmona"},{id:"305463",title:"BSc.",name:"Daniela Alexandra",surname:"Bernabe-Sanchez",slug:"daniela-alexandra-bernabe-sanchez",fullName:"Daniela Alexandra Bernabe-Sanchez"},{id:"305464",title:"BSc.",name:"Marissa",surname:"Limón-Cantú",slug:"marissa-limon-cantu",fullName:"Marissa Limón-Cantú"},{id:"305466",title:"BSc.",name:"Benjamin",surname:"López-Silva",slug:"benjamin-lopez-silva",fullName:"Benjamin López-Silva"},{id:"305467",title:"Dr.",name:"Martha Lucia",surname:"Ita-Amador",slug:"martha-lucia-ita-amador",fullName:"Martha Lucia Ita-Amador"}],corrections:null},{id:"69381",title:"Evolution of Parasympathetic Modulation throughout the Life Cycle",doi:"10.5772/intechopen.89456",slug:"evolution-of-parasympathetic-modulation-throughout-the-life-cycle",totalDownloads:735,totalCrossrefCites:0,totalDimensionsCites:2,hasAltmetrics:0,abstract:"Based on the largest data set ever available for analysis of heart rate variability (HRV) variables, in healthy individuals, it was possible to determine the evolutionary behavior of three representative components of parasympathetic nervous system function (RMSSD, PNN50, and HF ms2), in different age groups of the life cycle: newborns, children and adolescents, young adults, and, finally, middle-aged adults. A near-parabolic and nonsynchronous behavior was observed among the different variables evaluated, with low values at first, then progressive elevation, and later fall, approximating the values of the newborns to the values of middle-aged adults and suggesting that the autonomic nervous system, at least relatively to its parasympathetic component, undergoes a growing maturation that is completed in the young adult and later suffers a progressive degeneration, completing the life cycle. This fact should be considered when comparing the analysis between healthy individuals and those with different states of pathological impairment.",signatures:"Moacir Fernandes de Godoy and Michele Lima Gregório",downloadPdfUrl:"/chapter/pdf-download/69381",previewPdfUrl:"/chapter/pdf-preview/69381",authors:[{id:"305849",title:"Dr.",name:"Moacir",surname:"Godoy",slug:"moacir-godoy",fullName:"Moacir Godoy"},{id:"305851",title:"Dr.",name:"Michele",surname:"Gregório",slug:"michele-gregorio",fullName:"Michele Gregório"}],corrections:null},{id:"69583",title:"The Role of Magnetic Resonance Imaging (MRI) in Autonomic Nervous System Monitoring",doi:"10.5772/intechopen.89593",slug:"the-role-of-magnetic-resonance-imaging-mri-in-autonomic-nervous-system-monitoring",totalDownloads:744,totalCrossrefCites:0,totalDimensionsCites:0,hasAltmetrics:0,abstract:"Medical imaging of the nervous system is the methodology used to achieve pictures of parts of the nervous system for therapeutic uses to recognize the ailments. Magnetic resonance imaging (MRI) is a kind of medical imaging tool that utilizes solid magnetic fields and radio waves to deliver point-by-point pictures of the inside of the body. There are large number of imaging methodologies done each week around the world. Medical imaging is developing rapidly due to developments in image acquisition tools including functional MRI and hybrid imaging modalities. This chapter abridged the role of magnetic resonance imaging (MRI) in autonomic nervous system monitoring. This chapter also summarizes the image interpretation challenges in diagnosing autonomic nervous system disorders.",signatures:"Yousif Mohamed Y. Abdallah and Nouf H. Abuhadi",downloadPdfUrl:"/chapter/pdf-download/69583",previewPdfUrl:"/chapter/pdf-preview/69583",authors:[{id:"274452",title:"Dr.",name:"Yousif",surname:"Abdallah",slug:"yousif-abdallah",fullName:"Yousif Abdallah"},{id:"306956",title:"Dr.",name:"Nouf",surname:"Abuhadi",slug:"nouf-abuhadi",fullName:"Nouf Abuhadi"}],corrections:null}],productType:{id:"1",title:"Edited Volume",chapterContentType:"chapter",authoredCaption:"Edited by"},subseries:null,tags:null},relatedBooks:[{type:"book",id:"7290",title:"Special Topics in Resuscitation",subtitle:null,isOpenForSubmission:!1,hash:"5cc25d9b8a8bec2e374939f147f4e007",slug:"special-topics-in-resuscitation",bookSignature:"Theodoros K. 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This paper contains a discussion and review of safety, security and resilience of smart cities, considered as software ecosystem (SEC). The purpose is to provide an overview of research in the field, identify emergent risks in a systemic perspective and identify possible issues that existing literature is not addressing adequately. The article is initiated by a discussion of the concept of software ecosystems and the need for safety, security and resilience in smart cities.
In Ref. [1] there is a fairly general definition of a smart city, described as a place when investments in human and social capital and traditional (transport) and modern (ICT) communication infrastructure, fuel sustainable economic growth and a high quality of life, with a wise management of natural resources, through participatory governance. From [2], looking at specific systems, smart cites are described as a city that monitors and integrates conditions of its critical infrastructures, traffic (including roads, bridges, tunnels, rails, subways, airports, seaports), communications, water, power and major buildings. All this is done in order to optimize resources, plan its preventive maintenance and monitor security aspects while maximizing services to its citizens.
A literature review of software ecosystems in general was performed in [3] identifying 90 papers in the period from 2007 to 2012. The review identified the software ecosystem (SEC) as a fruitful systemic perspective. The review inspired us to find papers discussing safety, security and resilience of SEC published in the period from 2007 to 2016.
A software ecosystem (SEC) describes the complex environment of a smart city. A SEC will consist of components developed by actors both internally and externally, and solutions will spread outside the traditional borders of software companies to a group of companies, private persons and entities. In [3] they defined a software ecosystem as: “
When discussing software ecosystems, we include the legal and organizational framework in addition to applications and supporting infrastructure as described in Figure 1. Scope of digital ecosystems.
Scope of software ecosystems.
Software ecosystems are often based on the internet as infrastructure. The internet economy makes up a significant part of the GDP in 2016 since it is 5.3% of GDP [4]. SEC has gained more importance due to mobile platforms such as iPhone and android. Examples of SEC are:
Digital learning environments;
Mobile systems (phone applications);
Shopping and payments systems;
Social networking systems;
Personal wellness and healthcare (training, food, medical equipment and surveillance…);
Smart cities with transportation, infrastructure control (water, power). A part of Smart cities is intelligent transport systems (ITS) controlling vehicles, traffic management systems, electronic payments…;
“Smart farming” with systems to track livestock and harvest/yield; outside cities.
Arguments for discussing software ecosystems has been the speed of development; increased competition and reduction of development costs due to the opening up of development outside of organizational silos. Some of the software ecosystems are critical, in that a malfunction can severely affect the functioning of society or personal well-being. Examples are systems used in transportation, car control systems and health systems (such as pacemakers).
In this paper we have used the definition of safety as a state, as described by Department of Defense - [5], “
Security is used to describe conditions of intentional harm. The relationships to safety are discussed in [6]. Security is defined as “
In [9], the following definition of risk is given, “
Systemic risk is defined as “
A key element when assessing systemic risks are the scope and prioritization of systems to be evaluated. We have focused on critical systems of common interest in a city. In the following we have discussed risks and protection of what is defined as part of critical infrastructure. Definition and protection of critical infrastructure has been a key concern in the US and EU. In the US the establishment of the national infrastructure protection plan (NIPP) from 2009 has been updated systematically. The latest, [11], has the title “Partnering for Critical Infrastructure – Security and Resilience.” The successive NIPP has identified specific areas of concern such as interdependencies, cyber security and the international nature of threats. The risk management framework of NIPP is interesting since it is broad and systemic including physical, cyber and human elements. In the EU, the directive 114/08 on the identification and designation of European critical infrastructure and the assessment of the need to improve their protection was established as a council directive in 2008 [12]. In Table 1, we have described critical infrastructure sectors.
US-NIPP sectors | EU 114/08 sectors |
---|---|
Energy | Energy—electricity, oil, natural gas |
Transportation systems | Transport—roads and highways, railroads, aviation, inland waterways, shipping and ports |
Agriculture and food; bank and finance; communications; military installation and defense; technologies of information; national monuments and icons; drinking water treatments plans | (NA—not applicable yet) |
Critical infrastructure sectors in US-NIPP and EU 114/08.
The main elements and areas of this list of critical infrastructure, is highly relevant when discussing smart cities, of special interest are smart city applications related to: Transportation systems, energy systems (power supply), bank and finance; communication systems; Technologies of information (including navigation systems); Water supply and health systems. The following areas are critical when impacted by loss or failures (Table 2).
Areas impacted by smart cities | Examples of critical loss or failures |
---|---|
Transportation systems—Intelligent transportation, management and control of transport being impacted by surveillance, Google Map used to recommend routes, autonomous transport, traffic control centers managing transport and road signals | Breakdown of transport; impacting emergency services (police, fire, ambulance) or flow of material. (trough exploiting vulnerabilities in autonomous car systems; or influencing traffic control systems/halting control systems) |
Energy systems—smart metering and improved management through centralized or more technology-based power grid systems | Breakdown of power supply – breakdown of power grids through exploiting vulnerabilities in new technology, on a control level and in smart metering systems |
Bank and finance—many areas—one example payments systems integrated in toll roads and parking to manage traffic (reduce traffic in selected areas) and to make parking more user friendly and efficient | Breakdown of payment systems, halting/delaying key services |
Communication systems and technologies of information (including navigation systems)—autonomous cars, traffic control, route planning and signaling systems dependent on information technology and navigation systems. | Breakdown (accidents) in transportation due to nonfunctioning supporting technology |
Water supply—managed and optimized by control systems | Breakdown, contamination of water supply due breakdown (hacking) of control systems |
Health systems—dependent on sensors (such as in pacemakers) and communication systems (sending and receiving data from health professionals), “just in time” management of health, | Breakdown/errors in health systems used to manage critical operations, such as in peacemakers |
Systemic risks in smart cities.
The criticality or potential loss due to failures, breakdowns or attacks increases the need to be able to support critical operations even when the system is under stress or may fail, thus the ability to handle unanticipated incidents (or ability to go to a safe and secure state) are gaining importance. The concept of resilience engineering is an important strategy to handle these unanticipated incidents. In [13] resilience is defined as “
In the European Union, safety, security and resilience are prioritized in the cybersecurity strategy [15]. Three of the top five strategic issues mentioned are: Develop the industrial and technological resources for cybersecurity; Achieving cyber resilience; and establish a coherent international cyberspace policy for the EU. Thus, safety, security and resilience of smart cities are important issues that should be explored further. In addition, it is important to understand how risk governance of smart cities is addressed and established in order to support a coherent cyberspace policy of the key issues.
Based on the preceding introduction, and the summary above, the three research questions we wanted to explore are:
RQ1: How is safety, security and risks of smart cities (software ecosystems of cities) framed and defined?
RQ2: How is risk governance of smart cities (software ecosystems of cities) addressed?
RQ3: What are key issues in Governance of the ecosystem?
In the following we have described some of the challenges and problems of these research questions and our methodology (i.e., approach).
There is often poor focus on emerging risks, safety and security. These issues have been identified late when vulnerabilities have been exploited and unwanted incidents have been published. The suppliers and vendors (software vendors) seldom has to pay for unwanted incidents even if they are due to poor quality issues in the systems such as safety, security or resilience. The bill has been given to the users, the organizations and/or society.
Critical infrastructure is in most cases regulated by the authorities. Safety and security regulation is often reactive, and lags technological innovation. New software is implemented and societal consequences are discussed later. Internet of things (IoT) is an example of new technology that are introduced in software ecosystems that may affect operations of critical infrastructure. IoT has introduced a broad set of vulnerabilities and can challenge safety, security and resilience of software ecosystems. As an example the Mirai botnet was used in a Denial of service (DoS) attack on the internet firm Dyn, Ref. [16], using unsecured devices on a large scale. The attack affected Dyn’s clients such as Twitter, Reddift, Spotify, and SoundCloud. The cyber-attacks caused outages across the whole East Coast in the US in October 2016. When discussing vulnerabilities in a software ecosystem such as in smart cities, one challenge is that there is not one single supplier, but a set of suppliers that must be involved. Incident handling moves to a broader area where it can be difficult to identify responsibilities and manage competencies. This is relevant, in [17] the author points out that there are serious vulnerabilities (poor quality control) in systems used in smart cities (i.e., traffic control systems), which could be used to cause traffic jams or collisions.
The literature review started by a keyword search based on combination of “software ecosystems” “smart cities” and “safety, security, resilience.” Using Google Scholar and then searching the ACM Digital Library, IEEE Explore, Springer Link and Science Direct. The literature body was selected based on that software ecosystems/smart cities and safety (security and resilience) was the main theme. In addition, papers were selected based on a set of criteria i.e., have been peer reviewed and published in a scientific context (journal, conference), available in English, and more than one-page long. Since software ecosystems involves governmental rules, relevant white papers were also identified. The identified literature body is gathered in Section 5, numbered from [18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29] [LIT BODY:13] and [LIT BODY:14]. In addition, we have listed other general references that could not be included in the literature body, in Section 6.
The concept of Risk and Risk Governance has been an issue in the review, and we have structured papers based on risk governance, see [30], starting with problem framing; then risk appraisal (hazards and vulnerabilities); risk judgment; risk communication and risk management.
We found 14 papers in total, 13 papers published in the interval 2007–2016; and we included a paper from 2003 that had an illuminating discussion of resilience of systems. The following three sections are based on our research questions (RQ1 to RQ3 as described in Section 2) and have been used as title of the chapter:
Framing of safety, security and risks in smart cities (RQ1)
Risk Governance of smart cities (software ecosystems) (RQ2)
What are key issues in Governance of the ecosystem? (RQ3)
In [31] there is a discussion of the convergence of safety and security, pointing out that a successful integration of both requirements needs the collaboration of both safety and security disciplines, aided by a common understanding. In [28, 32], it is pointed out that both safety and security issues must be assessed to build trustworthy software ecosystems. Issues identified through security analysis (i.e., threats) must be combined with issues from safety analysis (i.e., hazards). In [33] there is a focus on of the development of industrial control systems and how safety and security must be integrated in the development methodologies. These control systems are similar to control systems employed in smart cities. An overview and comparison of methodologies is given.
In [34], a broad overview of security and safety challenges of digital systems are given based on an ecological perspective. Ecology is used both as a metaphor to learn from the development in the nature, but also to have a more holistic perspective of systems involving human actors in a society. The ecosystem perspective is as an important viewpoint when discussing safety and security in a changing word, and especially when exploring risks and risk governance of smart cities.
In [35] there is a discussion of infrastructure resilience from an organizational context. Adaptive capacity, resource robustness is discussed related to infrastructure and a conceptual framework for assessing resilience is outlined. The conceptual framework seems to be useful when discussing resilience in software ecosystems, especially of critical (infrastructure) ecosystems. In [36] different elements of resilience are discussed. The paper presents a framework for system resilience, consisting of five aspects: time periods, system types, events, resilience actions and properties to preserve. It is followed by principles for emergence, and factors affecting resilience, including improving resilience, trade-offs, and loss of resilience.
Not many textbooks (that can be used in teaching) have been found related to implementation of security and resilience in control systems of smart cities. However, in [37] guidelines for secure and resilient software development are discussed. The development guidelines are targeted toward software ecosystems; and the goal is to improve developer skills related to security and resilience. It is pointed out that security and resilience must be integrated from concept/early design, it reviews security design methodologies and suggests how to measure the development process. The discussion of security in Industrial Automation setting, is discussed in [38], including the challenges of adapting general software security principles to industrial automation and control systems.
In [29] resilience and cyber security of the ecosystems is seen as a part of the maturity of governance and collaboration between industry and government. Thus, cyber resilience is seen as the next step of cyber security.
In [24] there is a discussion of the security dynamics of software ecosystem (SEC), pointing out that SEC reduces cost and are increasing efficiencies for the software producers while society get the costs of software failures (i.e., issues related to security, safety and poor resilience). The paper has a quantitative examination of 27,000 vulnerabilities disclosed over the past decade (1996–2008). The paper identifies the interest of several stakeholders in the market of software vulnerabilities such as the vendors, safety experts/consultants, security information providers (SIP), and criminals. The paper explores several policies such as security trough obscurity, responsible disclosure of vulnerabilities (as a suggested policy) or security trough transparency. One of the key insights is that secrecy prevents people from assessing their own risks, which contributes to a false sense of security. The process of responsible disclosure is that the researcher discloses full information to the vendor, expecting that a patch is developed within a reasonable timeframe. An increasing number of vendors and security organizations have adopted some form of responsible disclosure. The role of security information providers (SIP) as risk-communicators is discussed in the vulnerabilities market.
In summary, there has been a positive development in identifying the need to explore both safety and security in development and to use resilience as a mitigating strategy. The concept of software ecosystems benefits the developers and industries, but it seems that at present that society gets the costs of software failures. Responsible disclosure of vulnerabilities to the vendors, expecting a patch, seems to be a beneficial policy. The role of actors in the software ecology, such as security information providers should be explored further.
In [26] a set of vulnerabilities in cars are pointed out such as the possibility to control a wide range of automotive functions and completely ignore driver input from dashboard, including disabling the brakes, selectively braking individual wheels on demand, stopping the engine, and so on. Attacks were easy to perform and the effects were significant. It is possible to bypass rudimentary network security protections within the car, and perform attack that embeds malicious code in the car that will completely erase any evidence of its presence (after a crash). There is a discussion of the challenges in addressing these vulnerabilities while considering the existing automotive ecosystem.
In [27] Semi-autonomous and fully autonomous cars are described as coming from the development stage to actual operations. The autonomous systems are creating safety and security challenges. These challenges require a holistic analysis, under the perspective of ecosystems of autonomous vehicles. The perspective of ecosystems is seen as useful to understand and mitigate security and safety challenges. These systems will become important critical information infrastructures, simultaneously featuring connectivity, autonomy and cooperation. Threat analyses and safety cases should include both (random) faults and (purposeful) attacks.
In [39], there is a discussion of Cyber-Physical infrastructure risks in the future smart cities. Several examples of unwanted incidents are described in transportation systems (autonomous vehicles; Trains; …) in electricity distribution and management and in the water and wastewater systems sector. It is suggested to the regulator to work with standards and regulations in addition to communication and increased engagement by giving direct assistance. Challenges mentioned are the need to establish goal based standards and regulations as new technology is implemented and to focus on dissemination of best practices in combination with systematic education.
In [17] there is an empirical evaluation of “smart cities” looking at a broad set of technologies of traffic control, management of energy/water/waste and security. Known vulnerabilities are in traffic control systems, mobile applications used by citizens, smart grids/smart meters and video cameras. The issues are in line with peer-reviewed papers, i.e., lack of cyber security testing and approval, lack of encryption, lack of City Computer Emergency Response Teams (CERT), and lack of cyber attack emergency plans. There are reasons to anticipate that we establish potential for serious incidents, if these issues are not addressed and mitigated.
In [20] there is a discussion of the expanded use of federated embedded systems (FES) in automotive and process automation. Expected benefits include the possibility of third-party actors developing add-on functionality; a shorter time to market for new functions; and the ability to upgrade existing products in the field. This is a substantial area for innovation and change, the responsibilities of the manufacturer will change, and a key challenge will be ecosystem management. However, it is suggested that the liabilities and responsibilities of the total product must rest with the manufacturer. The regulator has a key role to define responsibilities. These issues highlight the need for Risk Governance of systems to be used in smart cities.
In [21] open software ecosystem is proposed as an approach to develop software for embedded systems in the automotive industry. The focus is on the need to deliver functionality to customers faster. The paper describes quality attributes and defines a reference architecture. Both safety, security and dependability are explored.
In [22] they model the architecture of a cloud-based ecosystem, showing security patterns for its main components; and discuss the value of such an approach. The ecosystem approach provides a holistic view and is valuable in security, by indicating places where security mechanisms can be attached. Holistic views are seen as important to combine quality factors such as safety and reliability with security. By using this abstraction level, it is argued in the paper that this unified approach reduces complexity, one of the important weaknesses used by attackers and can enable analysis of the propagation of threats and data leaks.
In [28] they cover research on Enterprise Architectures of ecosystems (i.e., software ecosystems) discussing resilience and adaptability as a key area and suggest reference architectures mentioning security. However, safety is not mentioned.
In [25] there is a discussion on how to build robust and evolvable resilient software systems, discussing redundant data structures, transformer middleware and service-oriented communities. The use of transformer middleware may lead to more complex systems and higher costs or latency. Exploration of service-oriented communities may support adaptation and spontaneous emergence of resilience, but may lead to higher costs due to high degree of redundancy and challenges with deterministic behavior.
In summary, there has been documented several vulnerabilities in smart cities, intelligent transport systems and autonomous cars. However, software ecosystems have beneficial elements since more actors are developing functionality and enabling a shorter time to market. Liabilities must rest on the manufacturer and the regulator must define responsibilities. The ecosystem provides a holistic view that is seen as important to combine safety and reliability with security. It is argued in several papers that this approach reduces complexity; one of the weaknesses used by attackers and can enable improved analysis of propagation of threats and data leaks.
International governance of security of the infrastructure of software ecosystems is addressed through several channels such as standards (ISO, IEC) or international bodies such as OECD, EU, NATO and UN. Software Ecosystems are international—involving many actors with different agendas. In [40] there is a discussion of governance of emerging technology (such as IoT) as it is integrated into critical infrastructure. It is suggested that manufacturers should follow the principle of privacy and security by design, when developing new products, and must be prepared to accept legal liability for the quality of the technology they produce. Buyers should collectively demand that manufacturers respond effectively to concerns about privacy and security. Governments can play a positive role by incorporating minimum security standards in their procurement. It is suggested that government regulations should require routine, transparent reporting of technological problems to provide the data required for a transparent market-based cyber-insurance industry. It is suggested to establish an agreement (a compact) based on collaboration between government, industry and private society supporting evidence based decision making.
In [19] the focus is on software assurance of safety-critical and security-critical software (i.e., conceptualized as SEC). The perception is that the use of current methods has not achieved the wished-for level of protection, and that there are missing security principles and standards. The industry continues to see an expansion of major breaches occurring in both the public and private sectors. There need to be incentives or regulations for implementing protective and immunizing measures. Such measures could be a mandatory part of the security architecture of all applications. A formal requirement could be that implementation of protective and immunizing measures is included in any certification process. On governance it is suggested to establish software assurance standards at the UN level; to have a risk based approach; to share best of breed methods; and the need to discuss liabilities for damages occurring as a result of an attack or security-related errors.
In [18] the issue of Information security is highlighted in national governance. They propose a comprehensive conceptual framework for building a robust, resilient and dependable Information Security Infrastructure, based on the perspective of software ecosystems.
Development of security and resilience is seen as a maturity process in [41], referencing the CERT Resilience Management Model (CERT RMM) from the Carnegie Mellon Software Engineering Institute. Resilience as a strategy is not simple to implement, in [42], the analysis of resilience strategies in the US agencies revealed that most of the plans only focus on a few of the stages of resilience. Plans do not focus on resilience in the information and social domain, and do not consider long-term adaptation.
In [23] there is a discussion of resilience as a high level design principle. There is an argument for resilience in systems, i.e., distributed systems composed of independent yet interactive elements may deliver equivalent or better functionality with greater resilience. Guidelines for resilience are given such as robustness through resilience rather than resistance, and intervention rather than control. It is argued for the perspective of resilience and to use an ecological perspective in system design and deployment, thus this article describes a design methodology on the ecology level based on resilience principles.
In [43] there is a discussion of development of software-systems, and ignoring some perspectives of software ecosystems. If we want systems that are secure and reliable, both security and reliability must be built together. Applications, middleware and operating systems must be built in the same way, to get systems that are inherently secure and that can withstand attacks from malicious applications and resist errors. The suggested approach is based on security patterns that are mapped through the architectural levels.
The papers identified that the risk assessment was complex, thus there is a need to use methods that integrates the following issues:
Technology, ensuring that scope of methodology includes safety issues (such as described by IEC 61508 - Functional Safety of Electrical/Electronic/Programmable Electronic Safety-related Systems) security issues (ISA/IEC-62443 to ensure secure Industrial Automation and Control Systems) in addition to a Certification Framework such as the European IACS components Cybersecurity Certification Framework (ICCF).
Human Elements: Risk understanding and perceptions of the involved actors, including understanding of both safety issues and security issues
Organizational issues, ensuring that responsibilities are in place, and that necessary organizational structures are in place both to specify, implement, operate and handle deviations critical components of the system.
In summary, if we want systems that are secure and reliable, both security and reliability must be built together. The suggested approach is based on security patterns that are mapped through the architectural levels of the system. However, there is missing international regulation or compacts based on private public partnerships to ensure privacy, safety, security and resilience. Vendors must ensure this quality by design, and must be prepared to accept legal liability for the quality of the technology they produce. Regulations should require routine, transparent reporting of technological problems to provide data for a transparent market-based cyber-insurance industry. There is an argument for resilience in systems, composed of independent yet interactive elements that may deliver equivalent or better functionality with greater resilience. However, the maturity of resilience in use is varying.
In this review, we have used the concept of software ecosystems on systems used in smart cities. Our review indicates that the “smart cities” concept are vulnerable and subject to increased emerging risks due to introduction of new technology (such as autonomous transport systems) unsecured components and new connections that has not been foreseen or thought of. Threats, new vulnerabilities and new unwanted incidents are emerging and can be observed through media attention and exploration.
Software assurance of safety-critical and security-critical software (conceptualized as the software system ecosystem) is strongly needed. Current methods have not achieved the necessary level of protection, and are missing security principles and standards. The industry continues to see an expansion of major breaches occurring in both the public and private sectors. Incentives or regulations are needed to implement protective and immunizing measures.
The ecosystem approach seems a promising approach since it provides a holistic view of security needs, by indicating places where security mechanisms can be attached. This approach reduces complexity; one of the important weaknesses used by attackers and can enable analysis of the propagation of threats and data leaks.
Due to the increased proliferation of the IoT and the vulnerability of the Internet, there is a strong need to establish a social compact (agreement) ensuring that the Internet continues to be accessible, inclusive, secure and trustworthy. To ensure that all actors in the value-chain understand the vulnerabilities and the risks, a silo-based “need to know” principle must be replaced by transparent and open reporting. This may support a market based cyber-insurance industry.
In the literature body and in [32] there is an increased understanding of the need for collaboration between the safety and security disciplines to understand and mitigate risks and vulnerabilities. The differences in perspectives between security and safety are due to different adversity models. The security community addresses threats (directed, deliberate, hostile acts) and the safety community addresses hazards (undirected events). Software ecosystems are so pervasive across all sectors of economic activity that this silo approach can no longer be regarded as acceptable.
There is a need for international rulemaking and regulation. This may be difficult to achieve. Vendors must ensure safety, security and resilience by design, and must be prepared to accept legal liability for the quality of the technology they produce. Prescriptive and detailed rulemaking on a national level is missing and is difficult to achieve. This is an international challenge. The Mira denial of service (DoS) attack was due to components produced in China but used in the US. No penetration testing, acceptance or testing of robustness was performed prior to release of the product.
In general, there is a need to establish functional standards, responsibilities of liabilities and practices cross-countries. There must be a specific responsibility of the producer to ensure safety, security and resilience, and ideally, a formal process of product acceptance or certification or safety case exploration before a product can be sold or offered. Thus, there is a need for regulatory action from government to set minimum standards, establish responsibility, and follow up of incidents/accidents. The suppliers should establish a proactive focus on (best practice) safety/security standards.
In Table 3, we have exemplified critical ecosystems such as smart cities/intelligent transport systems. Based on our review so far, these critical systems have no mandated test criteria (neither safety cases nor security cases, thus it is described as “Poor”) and there are no organizations such as CERTS to handle and systematize unwanted incidents.
Ecosystem | Vulnerability | Test | CERT |
---|---|---|---|
Smart cities and intelligent transport systems | Disruption of services (transport, power, water) | Poor | No |
Critical digital ecosystems and learning.
Development of safety has often been dependent on exploration of publicized accidents and incidents, and a systematic learning loop between users, the regulator and industry. An important component in the learning loop of software systems has been structured reporting and analysis of incidents trough computer incident response teams, i.e., CERTS. There is a need to regulate and ensure that new technology is approved/tested (has some sort of quality control/safety case examination) and that there is some sort of a structured learning process when incidents happen.
Software ecosystems will be exposed to new strains as new unsecured technology are introduced—thus there must be an increased focus on how to handle surprises i.e., resilience and adaptability in software ecosystems to ensure that new demands/stress/failures are not impacting the infrastructure in a catastrophic way. In the review of resilience, [44], there is an increased use of resilience in papers from 2006 on. The resilience concepts are in development, and there is a need to be careful not to place the responsibility of resilience on the individual (i.e., expecting resilience from an individual only). Resilience is the integrated ability of the ecosystem as a whole consisting of an interplay between technology abilities, organizational abilities and human abilities. During the review process, several issues have not been addressed adequately, and are in need of further research, such as:
There has not been an exploration of the different actors that can affect safety, security and resilience in smart cities (i.e., software ecosystems). Such an exploration should give insight into how to improve safety, security and resilience of systems, and how liabilities should be placed
There has been no systematic discussion of the maturation of resilience in smart cities (specifics in software ecosystems) discussing technology, organizations and human awareness/human actions together
There have been few definitions of patterns of resilience in smart cities and related software ecosystems and how these can be used at an architectural level. There is a missing discussion on how smart cities/critical ecosystems can become resilient, based on patterns
How to perform ecosystem management of development of federated embedded systems (FES) used in smart cities (i.e., transportation, automotive systems…)
Almost one of every three adults worldwide dies because of cardiovascular diseases (CVD), making them the most prevalent cause of morbidity and mortality [1]. Several factors increase the risk of suffering a CVD. They can divide into two groups: modifiable and non-modifiable [2]. The former are those factors that can be controlled and modified by behavior, such as physical activity and diet, while the latter ones cannot be changed, like age and genetics. Environmental factors include air pollution and exposure to heavy metals, such as arsenic or lead, and the WHO recognizes them as important CVD risk factors. They could be considered “modifiable”; however, considering that most of the population affected by environmental pollution live in medium to low-income countries, their modification might be complex. An excellent review on this topic was published elsewhere [3]. The apparition of pathological conditions during pregnancy such as pre-eclampsia [4], maternal supraphysiological hypercholesterolemia (MSPH) [5], or gestational diabetes mellitus (GDM) [6] alters the fetal environment and is associated with an increase an increased risk of CVD in the offspring. They might be considered “between” modifiable and non-modifiable: In the gestational state, controlling the disease might prevent the fetal vascular impairment; however, after birth, there is a lack of evidence regarding treatments for improving their outcome and might be considered a non-modifiable factor. Most of the published research focuses on the repercussions of maternal health after suffering pregnancy disease [7, 8]. Still, their effects on the cardiovascular health of the fetus have been less described.
Over the last decades, the evidence associating pregnancy diseases and fetal outcomes has grown. Regarding MSPH, the apparition of fatty streaks on tunica intima of large arteries at fetal stages [9], probably related to alterations in nutrient transfer through the placenta [10], increases the risk of future cardiovascular events. Sadly, this condition is frequently underdiagnosed [11], and for a solid understanding of its prognosis more studies are needed. Preeclampsia is a relatively common complication of pregnancy [12]. It is associated with a slight but sustained increase in diastolic and systolic pressure on the offspring that seems to maintain for life [13, 14]. Preeclampsia also is related to Intrauterine Growth Restriction [15], which, in turn, is associated with an impaired vascular and metabolic condition [16], predisposing the offspring to worst cardiovascular outcomes. Finally, GDM is a more common disease with global prevalence between 6 and 7% (Europe and United States) and 9 and 13% (South and Central America, Asia, Africa) [17]. The prevalence over the last decades has been increasing in most countries [18, 19, 20, 21]; this might relate to the increase in maternal body mass index and the age of a pregnancy [18]. In terms of fetal cardiovascular impairment, a recent meta-analysis found that the offspring whose gestation was affected by GDM present higher basal glucose and systolic pressure [6]. In another large study, GDM pregnancies increased the prevalence of early-onset CVD by almost 30% in the offspring [22]. This worldwide statistical information urges researchers and clinicians to study the repercussions of GDM-complicated pregnancies further. Even more, an association between GDM and preeclampsia has been recently described [23, 24]. This relation can be explained at a systemic level by the increase in the age at which women become pregnant and the augment in body mass index told before; besides, both are related to damage on endothelial cells (EC), impairing vascular homeostasis [23]. Finally, between GDM and MSPH, a relation was recently suggested [25, 26], where EC in the placental vasculature and trophoblasts might have a crucial role; however, there is a considerable lack of evidence in this regard. At this point seems fair to suggest that EC is essential for the pathological development of the three conditions mentioned above. We will explore the GDM-induced vascular and trophoblastic injury and how it can probably impair fetal vascular health in the following pages.
GDM is the apparition of spontaneous hyperglycemia in pregnancy without the previous diagnosis of a condition whose main feature is insulin resistance (IR) [27]. This definition is consistent with the evidence that GDM pathophysiology differs from pregnancies of women with prior diabetes in multiple aspects [28] as discussed later.
During a healthy pregnancy, the peripheral insulin sensitivity variates: In the early gestation increases to promote the fill up the glycogen and adipose stores [29], later it declines [30], increasing maternal systemic and placental glycemia. This reduction of insulin sensitivity (i.e., IR) occurs due to the pregnancy variation of systemic and placental hormones (for example, leptin, cortisol, estrogen, progesterone) [31] and is matched with a 2-fold increase in insulin secretion from pancreatic β-cells [32]. Late gestational hyperglycemia favors the transport of glucose to the fetus; however, it depletes the glycogen reservoirs and induces the use of fatty acids as fuel [33]. In GDM, maternal insulin sensitivity almost halves [34], implying two consequences: less accumulation of glycogen in both muscle and liver in the early pregnancy and faster use of them during late pregnancy. Furthermore, once the glycogen stores deplete, the use of fatty acids to obtain energy is more pronounced than in physiological pregnancy, leading to hypertriglyceridemia (HTG) (Figure 1).
Metabolic differences between first and third trimester in healthy pregnancies, with a low degree of IR and previously diagnosed Diabetes mellitus. Previous low degree of insulin resistance increases the risk of developing GDM in the third trimester; however, since it courses without significant symptoms, previous IR repercussions are not usually assessed. PGDM alters the placenta’s formation in the first trimester, leading to more significant complications on the mother and the fetus in the third trimester.
Nonetheless, the reader is invited to reflect that a broad spectrum of clinical conditions related to the variable peripheral state of IR can exist [35, 36]. Finally, HTG and hyperglycemia alter placental vasculature [37] and fetal metabolic homeostasis [22, 38]. These features will be the focus of the following sections.
Even when most of the pathophysiological features are known, reaching a diagnostic criterion for GDM has been troublesome. Huhn et al. [39] recently published a review of this topic. To date, one of the most widely accepted definitions is from the International Association of Diabetes and Pregnancy Study Group (IADPSG) [40]. The American Diabetes Association (ADA) agreed with IADPSG; however, first, they suggested a more flexible criterion than IADPS [41]. Table 1 summarizes both.
Test | IADPSG | ADA |
---|---|---|
Fasting glucose | ≥92 mg/dL | ≥95 mg/dL |
1-h glycemia after OGTT* | ≥180 mg/dL | ≥180 mg/dL |
2-h glycemia after OGTT* | ≥153 mg/dL | ≥155 mg/dL |
Diagnostic values for GDM.
OGTT: oral glucose tolerance test after a charge of 75 g of oral glucose.
• Both entities consider that this evaluation must be performed between 24 and 28 weeks of gestation.
• The first sample must be taken after 8 h of fasting.
The main difference between IADPS and ADA criteria is that the former considers that only one of the mentioned values needs to be altered to diagnose GDM. At the same time, ADA suggests that at least two of them must be present to diagnose GDM [41]. This slight discrepancy seems to be clinically significant: IADPS diagnostic of GDM increases two-fold [42] or three-fold [43] compared to ADA; moreover, using the IADPS criteria for diagnosis and treatment improves the adverse fetal outcomes of GDM [42, 43]. In this regard, ADA recent guidelines validated and included the IADPS criteria for GDM diagnosis [44].
Women’s pregestational condition has historically complexed the study of GDM. GDM tends to appear in women with a previous degree of IR, and insufficient insulin synthesis or release from the pancreas before gravidity [40]. However, for decades, GDM was described as “any degree of glucose intolerance with onset or first recognition during pregnancy” [42, 45], regardless of the prior existence of unrecognized IR. This definition implies a severe limitation. The test for GDM is usually performed between the second and third trimester; but the screening for metabolic perturbances on women at fertile age, before pregnancy, are not actively pursued or a worldwide practice. In this regard, at the time of the GDM diagnose, there are two potential scenarios (Figure 1):
GDM “de novo”: the increase of IR at the third trimester will trigger the disease, leading both mother and fetus to a trimester of hyperglycemia and HTG.
PGDM: the entire pregnancy will occur under a higher IR state, only being detected (and treated) from the third trimester and onwards.
Both conditions are clinically different. For example, birth weight over 4 kg, known as macrosomia, is associated with several fetal metabolic complications [46]. GDM is a risk factor of macrosomia; however, it has been recently suggested that PGDM might cause more severe and frequent metabolic complications, including macrosomia, in the fetus than GDM [28, 47]. A possible explanation for this might rely on more prolonged exposure to higher IR consequences, such as hyperglycemia and HTG. HTG in pregnancy on its own is associated with macrosomia [48]; besides, increased blood glucose, the primary manifestation of both GDM and PGDM, is also associated with poorer fetal outcomes [6, 49]. Both cause oxidative stress [50, 51], cytokine release, and meta-inflammation [52] in the forming placenta, impairing its ultrastructure and the nutrient transport to the fetus. Nonetheless, PGDM will expose the placental vasculature since its early formation to HTG and hyperglycemia. In the next sections, we will extensively discuss this topic.
As stated before, hyperglycemia and HTG are characteristic features of GDM and cause vascular injury on the placenta. Same as what happens on type 2 diabetes mellitus, GDM altered glucose metabolism on placental vasculature increases the production of reactive oxygen species (ROS) leading to oxidative stress (OS) [53, 54]. OS, in turn, favors the activation of Nuclear Factor kappa Beta and other pro-inflammatory pathways [55]. In GDM, the placenta itself expresses inflammatory cytokines [56]. Inflammation and OS will further induce systemic and placental IR, reducing the entry of glucose to cells [32, 57], impairing glycogen synthesis at the muscle and liver, leading to hyperglycemia and HTG. This oxidative and inflammatory state will also induce endothelial dysfunction (ED) impairing the vascular response to tissular metabolic needs, altering nutrient transfer to the fetus, and increasing the expression of adhesion molecules. To understand better the pathophysiological features of GDM on placental blood vessels and how it impairs the fetal metabolic condition, it is necessary first to summarize the main characteristics of the human placenta.
In this section, we will explore the main features of placental development. For an in-depth study on this topic, the reader is invited to review the recent publication done by Turco et al. [58]. In brief, after the fertilization, the zygote will course with successive divisions forming the blastocyst, which will, in turn, adhere to the endometrium and invade it. The most external epithelial layer of the blastocyst will produce various trophoblast cell types and generate the primary syncytium below the implanted embryo [59]. The outer trophoblasts cells will differentiate and fusion, creating the syncytiotrophoblasts [60], whereas the inner cells will differentiate in cytotrophoblast. The syncytiotrophoblasts invade the endometrium and give rise to lacunas, spaces filled with maternal blood that will enlarge, merge, and develop the trabecular system of the forming placenta. The structure formed by both cell types around the lacunae is the primary villi. Later, the fetal mesenchyme will penetrate the villous core forming a structure known as secondary villi. Finally, vascular capillaries will appear within the center of fetal mesenchyme, forming the tertiary villi after the third gestation week. In the following weeks, angiogenesis predominates, increasing capillary density in the villi by developing new branches from preexisting vessels. Thus, the surface area for nutrient and oxygen exchange between the mother and the fetus increase [61]. At this point, in terms of vascular development, the placenta has reached its maturity (Figure 2). It is important to note that there are other essential structures in placentogenesis; however, they are beyond the scope of this chapter.
The human term placenta. Maternal blood reaches the intervillous space (lacunae) through spiral arteries. Then, nutrients and oxygen cross the cytotrophoblasts from the microvillous membrane to the basal membrane and gets to the fetal blood vessels.
Tertiary villi arise at half of the second trimester. The pathological difference between PGDM and GDM becomes essential at this stage: from the implantation, and onwards, PGDM will expose the trophoblastic layer to an insulin-resistant, hyperglycemic, and hypoxic environment. Exploring the detrimental effects of both conditions is complicated since it needs the interruption of the pregnancy in human studies. Nonetheless, recent data permitted insight into the alterations caused by GDM or PGDM on the early placenta.
Spiral arteries in the endometrium are invaded by trophoblasts and remodeled [62]. This remodeling turns them into a resistance vessel, favoring the fell of arterial pressure, increasing placental blood flow. This process occurs by a coordinated proliferation, differentiation, and invasion of the trophoblasts, further forming the placenta. Several growth factors, including insulin-like growth factor I (IGF-I), and II (IGF-II) among others, released from the same trophoblasts [63] and other placental cell types, stimulate this process [64]. The placenta of GDM is heavier than healthy pregnancies, at least from the second trimester [65] and onwards [66]. This process is not fully understood; however, some findings have elucidated the role of growth factors. Placentas of IR pregnancies have an increased number of cytotrophoblasts, syncytiotrophoblasts, and EC due to a higher proliferation rate [64]. Consequently, placental vascularization in GDM is also enhanced by increased angiogenesis [67]. Differences in expression and secretion of growth factors from GDM trophoblasts themselves seem likely [68]. This increase in proliferation and angiogenesis has been shown in term placentas [68, 69]; yet, a recent study found that high IR is associated with a decrease in trophoblasts’ proliferation and increased apoptosis on first-trimester placentas [70]. Another recent work suggested that hyperinsulinemia can also exert those detrimental effects [71]. Apoptosis is low in early healthy pregnancies placentas [72], progressively increasing until term [73]. On GDM, apoptosis analysis has led to conflicting results, showing a decrease [74] or an increase [75] in term placentas. Different technical approaches or the criteria used to diagnose GDM might explain these discrepancies; therefore, more detailed studies are needed. In summary, IR impairs the signaling of growth factors on vascular and trophoblast cells, diminishing the development and invasion respectively at the first trimester; however, as gestation progresses, more growth factors are secreted in a compensatory manner further increasing the size, weight, and the number of blood vessels in the placenta.
Among growth factors, IGF-I and IGF-II are potent stimulators of placental vascular growth, acting through their cognate receptor or insulin receptor. It is important to note that the insulin receptor has two isoforms: A and B. Isoform B presents a sequence of 12 amino acids in the α subunit that A does not have. This slight difference gives them different intracellular signaling and substrate affinity. Isoform A is associated with a mitogenic phenotype via mitogen-activated protein kinases (MAPK), while Isoform B induces metabolic modulation via protein kinase B (Akt). Moreover, IGF-II interaction with insulin receptor A induces cell growth and invasion, while insulin activity on the same isoform protects from apoptosis [76]. This differential action may explain the differences observed in the regulation of apoptosis and cell cycle described above. Exposure to increased insulin levels reduces the insulin receptor and IGF-I receptor’s signaling via insulin response element I and downstream targets such as Akt [63]. At this point seems fair to hypothesize that IR impairs placental vascular development by altering the insulin and IGF-I receptor signaling, dysregulating proliferation, and apoptosis. This impairment might explain the high immaturity level of the villous observed in the GDM placenta [77]. Concordant with this hypothesis, human umbilical veins endothelial cells (HUVEC) increase MAPK signaling probably via isoform A of the insulin receptor in GDM [78]. Insulin exposure reestablishes the downstream signaling and membrane expression of both isoforms [78], making it an attractive therapeutic alternative; however, the effectiveness of insulin is highly dependent on the previous IR state. Indeed, obese women that develop GDM respond worse to insulin treatment than lean, diminishing the insulin receptor presence at the membrane and lesser downstream signaling [79, 80]. It is important to note that maternal obesity does not mean necessary IR; however, since most studies do not present evidence from the pregestational state, this suggestion seems fair to be made. More studies are needed taking this consideration since insulin does not seem to be always the better option. An excellent review on this matter has been published elsewhere [81].
Finally, disruption of insulin and IGF receptors signaling, observed in IR states, is related to insufficient trophoblasts invasion, pregnancy-associated hypertension, and increased pregnancy complications, including abortion [63]. In this regard, insulin signaling in the placenta seems crucial and will focus on in the next section.
The human placenta has no autonomic innervation, so vascular tone regulation is performed by the myogenic tone and humoral and metabolic factors. Humoral factors include norepinephrine [82], renin-angiotensin system (RAS), and vasopressin [83]. The three of them impair invasion of the trophoblast in spiral arteries and alter placental vascular homeostasis. This phenomenon has been studied in pre-eclampsia; however, in GDM, there is a lack of evidence pointing to its potential pathological role. Strikingly, GDM increases the risk of pre-eclampsia from the first trimester and onwards [84]. Indeed, GDM curses with some of the same pre-eclampsia’s placental vascular complications (i.e., placental hypoxia and ED) [85]. In particular, maternal vasopressin does not seem to affect fetal blood flow [86], same as norepinephrine [87]. Nonetheless, the latter is related to a reduction in fetal oxygen delivery. This is likely to happen in pregnancies of women with prior diabetes [88] and GDM [89]: both conditions increase catecholamines plasmatic concentration in part because of hyperglycemia [90]. Moreover, norepinephrine augments IR [91, 92], and epinephrine diminishes insulin secretion from the pancreas [93]. In summary, upregulation of catecholamines in GDM negatively impacts placental vessel homeostasis; however, further studies are needed to explore this issue.
Several studies have highlighted the physiological role of the RAS system in placental development and function. A review in this regard has been recently published elsewhere [94]. In brief, the placenta presents all the components of RAS [95]. After implantation, tissular hypoxia induces syncytiotrophoblast formation, the remodeling of the spiral arteries, and angiogenesis. Angiotensin II receptor 1 (AT1R) expression is increased by hypoxia in trophoblasts and spiral arteries, augmenting the expression of angiogenic factors [96]. In healthy pregnancies, AT1R is highly expressed in the trophoblasts in the first and second trimester, declining its levels on the third [97]. However, if hypoxia persists, the expression of AT1R remains high until the end of the pregnancy [98]. As mentioned above, GDM incurs placental hypoxia, which might increase AT1R expression in trophoblasts [99], vascularity in the placenta and placental weight. AT1R expression due to GDM also increases in other vascular beds in rodent models, increasing vascular resistance and systemic arterial pressure [99]. Further, GDM increases the plasma concentration of angiotensin II (AGII), and permanent exposure to AGII induces vasoconstriction, diminishing placental blood flow and fetal oxygen delivery [100]. Also, IR in GDM may cause hyperinsulinemia, which in turn enhances the AT1R [101] and AGII [102] expression. In this regard, the relation between RAS and GDM seems to be even more complex. Higher plasma levels of soluble renin/prorenin receptor in the early pregnancy relate to an increased risk of developing GDM in late pregnancy [103]. This observation is in concordance with the fact that inhibitors of RAS, such as losartan, improve the vascular condition in human diabetes [104, 105] and rodent models of GDM [106]. Furthermore, GDM also increases the plasma concentration of aldosterone [107], an end product of RAS. Interestingly, hyperaldosteronism is associated with ED [108], which will be the subject of the following section. Nevertheless, to the best of my knowledge, this issue has not been assessed on fetoplacental vessels of GDM. Finally, increased AGII umbilical cord levels are associated with increased IR in GDM offspring [109]. Lesser perfusion of the β-cells can explain this due to vasoconstriction and a reduction of insulin sensitivity [110]. Indeed, blockade of RAS ameliorates IR [111]. Both processes converge in EC, where AGII increases ROS production, favoring oxidative stress (OS) [112]. In turn, GDM placenta incurs in OS [54], which impairs insulin signaling in multiple points and induces an inflammatory response mediated by Nuclear Factor kappa B, JNK, and p38 MAPK [113]. On the other hand, AT1R stimulation increases the apoptosis in villous explants and trophoblasts, which associates with pre-eclampsia [114], an event that might also happen in GDM; however, further studies are needed to explore this intricate process.
ED is characterized by imbalanced vasodilation and vasoconstriction, elevated ROS, inflammation, and a deficit of nitric oxide (NO) bioavailability [115, 116]. All these phenomena occur in the GDM placenta, leading to an increased vascular tone and reduced perfusion.
Arachidonic acid is the precursor of thromboxane A2 (TXA2), a vasoconstrictor, and prostacyclin, a vasodilator. The synthesis of both can occur in EC. TXA2 acts through the TXA2 receptor (TR), present in the human umbilical vein. Besides, non-enzymatic oxidation of arachidonic acid produces isoprostanes [117], which can also interact with TR and induce constriction. GDM placentas show an increased synthesis of isoprostanes [54], probably due to the increased production of ROS. In GDM [118] and preeclampsia [119] the prostacyclin/TXA2 ratio is lower in the placenta. Interestingly, OS in trophoblasts increases the concentration of TXA2 but not prostacyclin, pointing to ROS as the responsible for this mechanism that increases the vascular tone. Endothelium-derived hyperpolarization (EDH) is mostly unexplored in placental vessels, yet it may play a role in GDM placental vascular impairment. EDH exerts vasodilation via stimulation of the Ca2+-activated K+ channels, which hyperpolarize vascular smooth muscle cells (VSMC) [120]. It is hard to guess if GDM alters this mechanism. Preeclamptic pregnancies show a lesser EDH effect [121]; however, type 2 diabetes mellitus increases the EDH effect [122]. Further studies are needed to elucidate if EDH impairs or compensates ED in GDM.
Nitric oxide (NO) is probably the most characterized endothelium-derived vasodilator agent. Indeed, some consider that NO is the most potent vasodilator in the human placenta [123]. Due to its biological relevance, it is not surprising that its bioavailability is highly regulated. For instance, NO depends on the cellular intake of L-Arginine and the activity of the nitric oxide synthases. In EC, endothelial nitric oxide synthase (eNOS) is the primary source of NO, and cytosolic calcium, protein kinase A, and AKT favor the activity of this enzyme [124]. Insulin stimulates eNOS via AKT; besides, diabetes impairs this stimulation reducing eNOS activity, while reduction of NO induces IR, forming a vicious cycle [125]. On the other hand, NO acts on the VSMC, causing dilation via guanylyl-cyclase; however, it favors apoptosis [126] and inhibits proliferation [127] of the same cell type. VSMC apoptosis reduces the capability of resistance vessels to contract; in contrast, AGII favors proliferation via ROS activation of p38 MAPK [128]. Interestingly, a recent publication observed that GDM increases the insulin receptor isoform A and IGF 1R [129]. This gives consistency to the observations stated before: GDM enhances RAS and insulin receptor isoform A signaling in the placenta, both favoring the proliferation of VSMC; however, even when the machinery to produce NO upregulates in GDM [130], a reduction in its bioavailability is observed probably due to depletion by oxidative stress [131]. In turn, NO reduction inhibits apoptosis and further favors proliferation of VSMC, which will increase vascular tone, reduce perfusion, increasing hypoxia, and stimulate angiogenesis and even more OS. Nonetheless, even when consistent, this idea (Figure 3) needs further experimental support.
Mechanisms of GDM-induced endothelial dysfunction in the human placenta. Insulin resistance, hyperinsulinemia, hyperglycemia, hypertriglyceridemia (HTG), and high plasma concentration of free fatty acids (FFA) characterize GDM. These alterations induce vasoconstriction, hypoxia, and reactive oxygen species (ROS) production. ROS, in turn, will increase thromboxane A2 (TxA2) and isoprostanes in endothelial cells, further favoring vasoconstriction. ROS also upregulates the adenosine signaling, and the adenosine/L-Arginine/nitric oxide axis will be upregulated; however, insulin resistance diminishes endothelial nitric oxide synthase (eNOS) phosphorylation and nitric oxide (NO) production. Also, ROS will interact with NO and produce peroxynitrite, reducing NO bioavailability.
l-Arginine also determines the synthesis of NO by eNOS. l-Arginine is transformed in l-citrulline for NO production by eNOS [123]; so, NO production is dependent on intracellular l-Arginine content. Cationic amino acid transporter 1 (hCAT-1) is the main responsible for the entry of l-Arginine to the cell in the human [132]. Interestingly, insulin, OS and the activation of adenosine receptor A 2A (ARA2A) induce hCAT-1 expression [133]. In this regard, even when in GDM impairs insulin signaling, OS and the activation of ARA2A will favor the expression of hCAT-1 and secure the l-Arginine entry. OS can also induce the activation of adenosine receptor [134]. However, the insulin effect over hCAT-1 expression and activity has been described as requiring functional ARA2A in HUVEC [135]. GDM hinders adenosine transport to the cell, increasing its extracellular concentration [136, 137]. Extracellular adenosine will activate ARA2A, which will induce vasodilation [133]. Interestingly, adenosine can also interact with adenosine receptor A 2B (ARA2B), which is expressed in microvascular EC and induces angiogenesis [138]. The high adenosine concentration facilitates the ARA2B activation and may relate to the increased vascularization and weight observed in GDM placentas. A recent work has shown that adenosine induces fetal vessels constriction; however, GDM impairs its vasoconstrictor effect [139]. Going back to the above, even when the whole adenosine/l-Arginine/NO axis raises in GDM, the lesser bioavailability of NO impedes its biological effect. Likewise, NO deficit might explain why GDM reduces the insulin vasodilatory effect [131]. In this regard, endothelial dysfunction by GDM not only affects vasodilation but vasoconstriction as well, hindering the capability of the endothelium to regulate the vascular tone.
Finally, it is crucial to note that hypoxia [140] and hyperglycemia [141] induce OS. Interestingly, hyperglycemia on its own can induce hypoxia [142]. Mitochondrial impairment is probably the most important source of ROS in GDM; an excellent review has been made elsewhere [143]. Further, a recent work described mitochondrial dysfunction in cytotrophoblast and syncytiotrophoblast from GDM pregnancies. The latter seems to be more comprised in terms of ATP generation and increases the expression of antioxidants [144]. Nonetheless, this impairment is more profound when higher grades of IR are present [113] and the pregestational condition is highly relevant [143]. Insulin can increase the production of antioxidants; however, in GDM placentas, the expression of antioxidants is increased constantly [145], making them less responsive to future oxidants insults. Finally, ROS can react non-enzymatically with NO, producing peroxynitrite, which has been shown to inhibit mitochondrial respiration and damaged mitochondria [146], making a vicious cycle for ROS production.
Hyperglycemia and HTG are the most common metabolic alterations in GDM. Recent work evidenced that HTG in early pregnancy is related to IR, β-cell dysfunction, and hyperglycemia [147]. Umbilical cord blood analysis has demonstrated that GDM causes fetal hyperinsulinemia proportional to maternal IR [148]. Triglyceridemia remains unaltered, but LDL concentrations increase and HDL diminishes in cord blood of GDM deliveries and directly associates with macrosomia [149]. Intriguingly, triglyceridemia remains unaltered since maternal HTG is better related to macrosomia than hyperglycemia itself [150, 151, 152]. In this regard, the relationship observed between HTG and macrosomia in GDM might have two possible causes: an increase in the fetal delivery of free fatty acids (FFA) posterior to the action of lipases or the impairment of placental homeostasis due to ED. The first hypothesis does not seem likely: even when GDM curses with high FFA maternal plasma concentration [153], cord blood FFA content remains unaltered in GDM deliveries [154]. In this regard, the second hypothesis seems more plausible. HTG is related to ED; however, a mechanistic explanation is lacking to date. A recent review was made about this topic elsewhere [155]. A probable explanation for ED lies in macrophage activation by triglyceride-rich lipoproteins like Very-Low-Density Lipoprotein (VLDL) [156]. VLDL also induces ROS production and expression of inflammation mediators such as Tumoral Necrosis Factor α (TNF-α) in EC [157]. Interestingly, TNF-α favors IR and hyperinsulinemia in GDM [32], hindering insulin-mediated vasodilation. Also, the oxidative environment induced by triglycerides may favor the NO consumption, establishing the ED. Nonetheless, further studies are needed to address this issue in GDM placentas.
Finally, glucose transport in the placenta is regulated by maternal glycemia and by the expression and activity of glucose transporters (GLUT). For transportation from the mother to the fetus, glucose must go through the microvillous membrane (MVM), at the maternal side, to the basal membrane (BM) on the fetal side [158]. At least 6 GLUT transporters have been identified in the placenta: GLUT1, GLUT3, GLUT4, GLUT8, GLUT9, and GLUT12. Nonetheless, the most abundant isoforms in the placenta are GLUT1 and GLUT4. GLUT1 levels increase in syncytiotrophoblasts along with the pregnancy progression [159]. GLUT1 expresses in the MVM 3-fold than in the BM. Thus, crossing the BM is the rate-limiting step for glucose transport to fetal circulation [160]. Indeed, increased content of GLUT1 is correlated proportionally with fetal weight and macrosomia [161]. GLUT4 expression, contrarily to what was thought before [159], increases during gestation in the MVM, but only in healthy lean women [162]. In GDM, interestingly, insulin lowers mRNA of GLUT4; besides, various authors found increased GLUT1 expression [79, 163, 164]. Even more, GLUT1 upregulation is more profound in PGDM [164]. In this regard, it seems fair to suggest that GLUT 1 in the BM is critical for GDM pregnancy complications due to increased glucose transport [165]. Hyperglycemia should limit GLUT1 expression in trophoblasts and favor its movement from the membrane to the cytoplasm [166, 167]; however, in GDM, this does not seem to happen. A mechanistic study is necessary to address this issue. Finally, an increased transfer of maternal insulin to the fetus could explain hyperinsulinemia observed in the fetal cord of GDM deliveries. Nonetheless, near 1% maternal insulin crosses the placenta [168]. This could hardly cause an increase in fetal insulinemia; however, it may contribute. In this regard, the Modified Pedersen hypothesis offers a better explanation: Maternal hyperglycemia passes through the placenta to the fetus; then, from the second trimester and onwards, the fetal pancreas responds to hyperglycemia with hyperinsulinemia, further favoring glucose disposition in fat stores and the anabolic effects of insulin, resulting in macrosomia [169]. This could also explain the vascular alterations observed in the GDM offspring; however, further research for addressing this issue is needed.
GDM is a complex condition that affects both fetus and mother. Its impact on the offspring includes vascular and metabolic impairment before birth, predisposing them to early CVD. The real prevalence of GDM worldwide is unknown and might go beyond our expectations since it is mostly underdiagnosed. Moreover, the differential impact of previously diagnosed diabetes in pregnancy has begun to elucidate in the last few decades. On the other hand, the reader is invited to reflect that the pathological IR state in pregnancy is not a “black-or-white” matter but a continuous spectrum of possible conditions and fetal outcomes that needs to be assessed in every pregnancy individually. Including the assessment of HbA1c and lipid profile test in the first trimester, evaluation might improve the diagnosis of PGDM and foresee the future GDM development.
Previous IR state and PGDM hinder syncytiotrophoblast invasion in maternal vessels and the placenta formation; however, there is still much to research and learn from this subject. After development, GDM will continuously expose the placenta to a hypoxic environment that will impair vascular function due to increased OS and inflammation. HTG, hyperglycemia, and increased FFA will favor this pro-oxidant environment, causing ED. The regulation of the vascular tone by EC will impair favoring vasoconstriction and further tissular hypoxia. The nutrient transfer to the fetus will alter on this condition, exposing it constantly to hyperglycemia. Persistent hyperglycemia will damage its blood vessels and force its β-cells to secrete insulin extensively, causing metabolic and vascular impairment that will predispose it to CVD before its birth.
Especial thanks to Tamara Jiménez Iturrieta for the illustrations.
The author declares that no funding was received for this publication.
The authors declare no conflict of interest.
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He is an evaluator of project proposals for the European Union (H2020), Medical Research Council (MRC, UK), Spanish Government (ANECA, Spain), Research National Agency (ANR, France), DAAD (Germany), Argentinian Government, and the Colombian Institutions. He has been a reviewer in different indexed international journals (<70) and conferences (<250) since 2001. He has been a member of the IASTED Technical Committee on Image Processing from 2007 and a member of the IASTED Technical Committee on Artificial Intelligence and Expert Systems from 2011. \n\nHe has held the general chair position for the following: ACM-APPIS (2020, 2021), IEEE-IWOBI (2019, 2020 and 2020), A PPIS (2018, 2019), IEEE-IWOBI (2014, 2015, 2017, 2018), InnoEducaTIC (2014, 2017), IEEE-INES (2013), NoLISP (2011), JRBP (2012), and IEEE-ICCST (2005)\n\nHe is an associate editor of the Computational Intelligence and Neuroscience Journal (Hindawi – Q2 JCR-ISI). 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