Ransomware types and characteristics.
\r\n\t
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Venkateswarlu",coverURL:"https://cdn.intechopen.com/books/images_new/371.jpg",editedByType:"Edited by",editors:[{id:"58592",title:"Dr.",name:"Arun",surname:"Shanker",slug:"arun-shanker",fullName:"Arun Shanker"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"878",title:"Phytochemicals",subtitle:"A Global Perspective of Their Role in Nutrition and Health",isOpenForSubmission:!1,hash:"ec77671f63975ef2d16192897deb6835",slug:"phytochemicals-a-global-perspective-of-their-role-in-nutrition-and-health",bookSignature:"Venketeshwer Rao",coverURL:"https://cdn.intechopen.com/books/images_new/878.jpg",editedByType:"Edited by",editors:[{id:"82663",title:"Dr.",name:"Venketeshwer",surname:"Rao",slug:"venketeshwer-rao",fullName:"Venketeshwer Rao"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"4816",title:"Face Recognition",subtitle:null,isOpenForSubmission:!1,hash:"146063b5359146b7718ea86bad47c8eb",slug:"face_recognition",bookSignature:"Kresimir Delac and Mislav Grgic",coverURL:"https://cdn.intechopen.com/books/images_new/4816.jpg",editedByType:"Edited by",editors:[{id:"528",title:"Dr.",name:"Kresimir",surname:"Delac",slug:"kresimir-delac",fullName:"Kresimir Delac"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}}]},chapter:{item:{type:"chapter",id:"71371",title:"Ransomware and Academic International Medicine",doi:"10.5772/intechopen.91762",slug:"ransomware-and-academic-international-medicine",body:'\nHealthcare is among the leading industries targeted by cyber-criminals [1]. Malware, or malicious software, refers to programs designed to infiltrate computers without the users’ consent, and includes threats such as viruses and ransomware. Ransomware, a version of malware, exploits vulnerabilities to hijack target information technology (IT) infrastructures for monetary gain. Health information is an attractive target for cyber-criminals, as research suggests that an individual’s medical information is 20–50 times more valuable than personal financial information [1]. Access to medical information enables cyber-criminals to commit identity theft, medical fraud, and extortion, and illegally obtain controlled substances. The utility, versatility, and centralized storage of medical information, relatively weak IT security systems, and expanding use of healthcare IT (HIT) infrastructure all contribute to an increase in cyber-attacks on healthcare entities [1]. In fact, cyber-attacks targeting medical information are increasing ≥22% annually [1]. Depending on completeness, recency, and accuracy, a single patient’s file may fetch hundreds to thousands of dollars on the Dark Web [2, 3]. In Australia, it has been reported that the medical card number of every citizen is for sale on the Dark Web [3]. Moreover, attack-associated costs are reported to cost $1–3.7 million USD to clean up, with an average downtime cost per attack being $141,000 USD [1, 4, 5, 6]. A study by IBM and the Ponemon Institute reported that cyber breaches in the United States (U.S.) cost up to $6.2 billion per year and that almost 90% of hospitals have reported a data breach [7].
\nA literature search was performed of: China National Knowledge Infrastructure (CHKD-CNKI), Cochrane CENTRAL, CINAHL, Directory of Open Access Journals (DOAJ), Embase, Korean Journal Database (KCI), Latin American and Caribbean Health Sciences Literature (LILACS), IEEE-Xplorer, information/Chinese Scientific Journals database (CSJD-VIP), Google Scholar, Magiran, PsycInfo, PubMed, Scopus, Scientific Electronic Library Online (SciELO), Scientific Information Database (SID), TÜBİTAK ULAKBİM, Research Gate, Russian Science Citation Index (RSCI), and Web of Science (WoS). Relevant bibliographies were also searched. The search terms included the U.S. National Library of Medicine MeSH terms hospitals and computer security, as well as the terms ransomware, cyber security, web security, and healthcare.
\nRansomware utilizes malicious software to infiltrate computer systems or connected devices to encrypt a user’s files in order to carry out an extortion attack [8, 9]. Most commonly, ransomware infects a system when its user opens a compromised e-mail or visits a compromised website (i.e., drive-by downloads) [8]. Once downloaded, servers (i.e., web and e-mail), databases, end-user computers and removable media may become involved, including personal cloud storage services [2, 9]. The intended purpose of encryption is privacy, where someone with access to the encrypted data (“ciphertext”) is unable to discern its contents in a readable form (“plaintext”) [9]. There are two types of encryption, or cryptography: symmetric key and public key. In symmetric key cryptography, the sender and receiver use the same secret key to encrypt and decrypt the data. Public key cryptography uses a pair of keys: a public key (shared between both parties) and a private key (sender and receiver have their own unique private key) [9].
\nRansomware uses a hybrid encryption system that combines the two cryptographies to create an asymmetrical cryptosystem in which data are encrypted using a randomly generated symmetric key, which is subsequently encrypted using a public key where one party has the corresponding private key [9]. The cyber-criminal uses the private key to decrypt the symmetric key in order to decrypt the data back into “plaintext” and sends the key back to the victim, who can then use it to regain access to their system [9].
\nOnce encrypted, information becomes indecipherable and inaccessible. The user receives a pop-up notification demanding payment of a ransom (usually in untraceable digital currency such as bitcoin) in exchange for the decryption key [10]. Ransomware often does not destroy data, but rather, locks-up the data until a ransom is paid [11]. Even if the ransomware infection is removed, the data may remain encrypted [11]. But it is important to note, the mere infection of a machine with ransomware is not enough. The ransomware must communicate with a server to get an encryption key and report its results [11]. This requires a server hosted by a company that will ignore the illegal activity and guarantee the attackers anonymity (called Bulletproof Hosting) [11]. These companies are often located in China or Russia [11]. Attackers also use a proxy or virtual private network (VPN) services to further disguise their own internet protocol (IP) addresses [11]. Attack numbers have grown in part because malware authors have adopted an easy-to-use modular design of ransomware distribution [12]. This Ransomware-as-a-Service (RaaS) approach has become increasingly available, assisting technically naive attackers through simplistic distribution with phishing and exploitation kits, while employing a trustworthy business model [12]. RaaS is most easily accessed on the Dark Web [13], where prospective cyber-criminals are provided access to an affiliate console allowing them to walk-through the process of receiving their ransomware exploit kit, configure settings, target selection, and selecting ransom rates [13]. Metrics on malware instillations and success rates are also available [13].
\nRansomware can be divided into three basic types: crypto-, locker-, and wipe-ransomware (Table 1). Although crypto- and locker-ransomware represent the two main categories, current variants often incorporate traits from both [8]. Crypto-ransomware (most common) encrypts both files and data [11]. Thus, infected files remain inaccessible if transferred to another device [11]. Critical system files are typically spared, enabling the device to continue functioning, as it may be needed to pay the ransom [11]. Additionally, crypto-ransomware prefers bitcoin due to the increased privacy of cryptocurrency. However, owing to worries over law enforcement, bitcoin anonymizers and laundering services have emerged.
\nRansomware Type | \nExamples | \nCharacteristics | \nData recoverable by moving files to another device? | \n
---|---|---|---|
Crypto- | \nCryptolocker Cryptowall CTB-Locker KeRanger\na\n\n Locky Petya Santana TeslaCrypt TorrentLocker WannaCry | \nEncrypts files and data. Typically, does not target critical system files, thereby allowing the device to function as it may be needed to pay the ransom | \nNo | \n
Locker- | \nReveton | \nCreates a digital locker around the computer system to block user’s access. The data on the device are typically untouched | \nPossibly | \n
Wipe- | \nPetrWrap | \nEncrypts files and data. Does not unlock files or device after ransom payment | \nNo | \n
Ransomware types and characteristics.
Believed to be the first piece of ransomware to successfully infect Mac computers (running OS X).
Conversely, locker-ransomware (a less effective extortion tool) locks the device by creating a digital “locker” around the computer system to block access [8, 11]. However, unlike crypto-ransomware, the data stored on the device are typically untouched and can often be recovered by moving it to another functioning computer for access [11]. Moreover, users may be able to remove the locker-ransomware remotely and avoid paying the ransom [8]. However, if remote malware removal is unsuccessful, ransom payments are typically made through payment voucher systems or cryptocurrency [8]. For example, online betting services may accept the voucher codes as payment, subsequently transferring the money to prepaid debit cards [11]. Money mules are then used to withdraw the cash.
\nWipe-ransomware first appeared in 2017 with the PetrWrap attack that encrypted the target’s master file table (MFT) forcing the operating system (OS) to reboot [14]. Unlike crypto- and locker-ransomware, the files encrypted by wipe-ransomware do not unlock it after payment, effectively resulting in data loss [14].
\nBefore 2005, online payment methods were less readily available. Victims were instructed to pay ransoms by sending checks to offshore accounts, SMS text messages, prepaid cards, or even premium rate telephone numbers that earned money for the attacker [11, 15]. However, these methods were risky since they were traceable. In 2008, the largely anonymous cryptocurrency bitcoin came into use, facilitating expansion of ransomware attacks [11]. The use of third-party holdings companies such as PayPal has provided additional payment avenues [15].
\nSince one’s ability to pay may vary greatly by geography and local economy, ransomware uses dynamic geographical pricing. Once a computer or system is infected, the ransomware establishes contact with its command-and-control (C&C) server, reports the infected device’s IP address, and the C&C server returns a price for the country associated with that IP address based on a pre-populated database [11]. Additionally, criminals more frequently target businesses than individual users owing to greater potential for ransom extraction. It has been reported that about $10,000 USD may be the optimal business ransom as it is both low enough to pay, and low enough to generate reluctance on the part of law enforcement to investigate [11].
\nThe decision whether to pay the ransom is critical. The U.S. Federal Bureau of Investigation (FBI) does not recommend paying ransoms, as only 50% of victims ultimately regain access to uncorrupted usable data. Further, ransom payment incentivizes attackers to continue exploiting healthcare targets [16]. Even so, an estimated 40% of organizations choose to pay the ransom in hopes of recovering data accessibility and mitigating further losses [17]. This may be more likely to occur if the hospital has a questionable backup and no business continuity [13].
\nChoosing not to pay, however, comes with the added costs of extended downtime and recovery, which may approach 23 times the ransom cost [6, 18]. Smaller organizations have been forced to close after not paying the ransom [19]. The FBI estimated that in 2016 alone, ransomware-associated monetary losses exceeded $1 billion USD, with an average downtime cost per attack of $141,000 [4, 5, 6]. Ultimately, the decision of whether to pay the ransom is an individual one and depends on the unique circumstances and stakes of every incident.
\nThe targeting of healthcare by ransomware dates to 1989, when the Harvard-trained evolutionary biologist Dr. Joseph L. Popp used malware to prey on scientists and organizations interested in early acquired immunodeficiency syndrome (AIDS) research [1, 11]. Dr. Joseph Popp, a World Health Organization (WHO) consultant and AIDS researcher himself, mailed 20,000 floppy disks containing ransomware to a group of attendees at the WHO’s International AIDS conference [1, 11]. When inserted into the target’s computer, the virus (known as AIDS Program, AIDS Trojan, or PC Cyborg) infected the computer with a virus that lay dormant until the 90th time the system was re-booted, at which point a note would appear on the screen asking for licensing fees to be paid while it encrypted and locked computer files [8, 12]. A $189 USD ransom to be mailed to a physical mailing address was demanded to “renew the software,” or users must forgo further use of their computer [1, 8]. Although authorities apprehended Dr. Popp, his creation resulted in many derivatives that serve as a framework for modern cyber-criminals [1].
\nOver 15 years passed before the next instance of ransomware (GPCoder), which was delivered via e-mail [15]. Among the first major medical centers attacked was Hollywood Presbyterian Medical Center (2016), a 400-bed hospital in Los Angeles, California [1, 10, 11]. Rather than pay the initial $3.7 million USD ransom, the hospital reverted to paper records until they were able to negotiate the decryption key ransom payment down to 40 bitcoins (about $17,000 USD) [1, 10, 11]. However, this does not account for 10 days of lost revenue while the hospital’s systems were inaccessible, nor does it account for a damaged reputation in patient data security. Subsequent U.S. attacks have included academic, government, and private healthcare systems including: Alaska Department of Health Office of Children’s Services (Anchorage, Alaska); Appalachian Regional Hospitals (Lexington, Kentucky); Berkshire Health Systems (Pittsfield, Massachusetts); Emory Healthcare (Atlanta, Georgia); Hancock Regional Hospital (Greenfield, Indiana); Heritage Valley Health System (Pennsylvania); Medstar (Baltimore, Maryland); Kansas Heart Hospital (Wichita, Kansas); Keck Medicine of the University of Southern California (Los Angeles, California); Los Angeles Health Department (Los Angeles, California); Methodist Hospital (Henderson, Kentucky); National Capital Poison Center (Washington, D.C.); Princeton Community Hospital (Princeton, West Virginia); J.W. Ruby Memorial Hospital of West Virginia University (Morgantwown, West Virgina); University of Buffalo and State University of New York (Buffalo, New York); and Verity Medical Foundation (San Jose, California) [9, 10, 12, 20, 21]. Additionally, health insurance companies have also been targeted [7]. The Anthem Blue Cross insurance company (USA) had over 78 million medical records stolen in 2015 [7].
\nThis problem, however, is far from constrained to U.S. entities; it is global. On May 12, 2017, a ransomware (WannaCry) that utilized a stolen National Security Agency (NSA) tool that highlighted a vulnerability of the Windows OS (MS17-010) infected more than 300,000 computers in at least 150 countries [12]. Sixty trusts within the United Kingdom’s National Health Service (NHS) experienced system-wide lockouts forcing at least 16 hospital closures, ambulance diversions, inability to access patient records, patient care delays (canceled appointments and elective surgeries), and function loss in connected devices such as MRI scanners and blood storage refrigerators [3, 21, 22, 23]. Five hospitals, including Barts Health (Royal London Hospital), one of the main trauma centers in London, had to close their emergency departments [7]. Similarly, the Singapore Health System experienced a breach of over 1 million patient records, including those of the Prime Minister [7].
\nThe rise in healthcare attacks in the U.S. may be linked to the enactment of the Health Information Technology for Economic and Clinical Health (HITECH) Act of 2009 [24]. This identified healthcare organizations as potential cash cows for cyber-criminals. Prior to 2008, only 9.4% of hospitals had adopted a basic electronic health records (EHR) system [8]. By 2014, 75.5% of hospitals had adopted basic EHRs [8], and now approximately 95% use them [12]. Additionally, HIT including glucose meters, infusion pumps, and implanted medical devices are also connected to, and dependent on, the hospital’s network [12]. Moreover, healthcare systems are twice as likely to have Flash (Adobe Inc., San Jose, USA) installed and three times as likely to have Java (Sun Microsystems, Santa Clara, USA) installed, two plugins that can be exploited by hackers [8]. Healthcare organizations have been focused on healthcare, not cyber security, thus several issues have increased their vulnerability over time. While aiming to improve care efficiency, increasingly connected technology allowing for multiple ways to connect to easily accessible medical devices increases the likelihood of a breach [3]. Also, the interface between HIT systems and mobile general-purpose consumer devices (e.g., smart phones) increases the challenge to protect PHI. Moreover, no U.S. federal or state law requires encryption for PHI. Though encryption is encouraged, and often incentivized, nothing requires covered entities to utilize even the minimum standard of encryption [8]. Lastly, cyber-security funding is lacking, contributing to time lags between breech occurrence and detection [3].
\nImportantly, not all ransomware- and malware-generated traffic patterns are distinguishable from the normal traffic patterns generated by medical devices and systems with networking capabilities [21]. In this sense, both a malware encrypting a shared folder and an application compressing the same files have similar traffic patterns. Moreover, normal changes in the clinical environment may be misinterpreted as attacks if detection mechanisms adapt improperly [21]. Furthermore, malware developers are increasingly using encrypted traffic to avoid payload inspection [21]. Thus, achieving an acceptable balance between detection and false alarm rates remains challenging. A high false alarm rate may frustrate administrators and users, whereas a low detection rate may herald inefficacy.
\nDespite the growth of new technologies, many healthcare organizations persist in using legacy systems. For example, the use of Window XP (not supported since 2014) by some facilities allowed WannaCry to avoid detection [3]. Additionally, the proprietary nature of medical device software may prevent HIT teams from accessing internal device software, resulting in reliance on manufacturers to design and maintain effective device security [3]. Facilities in low- and middle-income countries (LMIC) may be at added risk owing to their use of open-source EMRs whose security may not be rigorously maintained.
\nLastly, outsourcing may play a role in healthcare organization vulnerability. Health insurance niche software and service vendors are offering outsourcing as a remedy for organizational cost controls [9]. However, offshore outsourcing companies are mostly self-regulated [9]. There is currently no standard as to how a healthcare provider may ensure that offshore business associates are adequately protecting the electronic PHI of their patients.
\nWith the dominance of ransomware as a leading cyber-security threat, it is important to consider its impact on International Health Security (IHS) [25]. Many countries lack the legal infrastructure to prosecute such crimes. Globally, cyber-attacks may result in substantial loss of resources, money, and life [26]. Although many security threats have emerged from LMIRs, many of these regions lag behind higher income regions in implementation of automated technologies and EMRs in the medical sector. That said, the IHS community is actively endeavoring to increase the availability and use of these technologies in LMIRs [27]. Thus, with falling costs and rising availability and implementation, HIT security will have an increasingly important role in IHS in upcoming years.
\nTraditional charting and management methodologies are steadily being replaced with digital ones. Technologies including digital algorithms and artificial intelligence are increasingly being used to monitor and coordinate threat responses [28, 29]. The IHS community has come to increasingly rely upon digital global surveillance networks such as the ProMED-mail (PMM) Network and the World Health Organizations (WHO) Global Outbreak Alert & Response Network (GOARN); systems that help organizations improve coordination speed and response time to temper the impact of international infectious disease outbreaks [30, 31, 32]. These systems are often used by IHS networks and volunteers in the field and, if compromised, could become a portal of entry for cyber-attack [31]. The attacks on the United Kingdom’s NHS demonstrate that even large state-sponsored institutions are not immune to cyber-attack [33].
\nLaboratory security is another important aspect for IHS, as the use and storage of sensitive pathogens make them attractive targets for attacks [33]. For this reason, the Global Health Security Agenda (GHSA) was created to help increase investment in global health security. GHSA is a 67-nation effort that hopes to increase the availability of laboratory systems for IHS use [34, 35].
\nAs with most HIT issues, preventing a ransomware attack is a complex socio-technical problem. Richard Schaeffer (2009), the U.S. National Security Agency (NSA) Information Assurance Director, testified to the U.S. Senate Judiciary Subcommittee on Terrorism, Technology and Homeland Security that 80% of all ransomware attacks could be prevented by adhering to security measures already in place [36]. In addition to a sophisticated encryption algorithm, ransomware attacks often rely on some form of “social engineering,” or the psychological manipulation of people to gain their trust and lead them to divulge confidential information [15]. Solving these problems is a shared task between HIT users and those responsible for configuring, maintaining, and operating the HIT infrastructure. While preventing all ransomware attacks is not possible, there are several steps that healthcare organizations can take to reduce risk and mitigate harm (Table 2). Additionally, the U.S. Department Health and Human Services (HHS) offer guidelines on the best policies on how to properly secure electronic PHI. The need to maintain software updates and patches cannot be understated. For example, Microsoft Inc. had released a patch for the vulnerability exploited by WannaCry and NotPeyta 8 weeks before the attack [8]. If systems had remained up to date, the impact of both malwares would likely have been significantly diminished.
\nDimension | \nRole | \nRecommendation | \n
---|---|---|
Leadership | \n\n
| \n|
Physical safeguards | \nPrevention and preparation | \n\n
| \n
Hardware and software | \nPrevention and preparation | \n\n
| \n
Incident Response | \n\n
| \n|
Clinical content | \nIntrusion detection | \n\n
| \n
User interface | \nEducation | \n\n
| \n
Prevention and preparation | \n\n
| \n|
Intrusion detection | \n\n
| \n|
People | \nEducation | \n\n
| \n
Identity and access management | \n\n
| \n|
Workflow and communication | \nIntrusion detection | \n\n
| \n
Risk assessment | \n\n
| \n|
Identity and access | \n\n
| \n|
Incident response | \n\n
| \n|
Internal policies, procedures and environment | \n\n | \n
| \n
External rules and regulations | \nPreparation | \n\n
| \n
Incident response | \n\n
| \n|
Measurement and monitoring | \n\n | \n
| \n
An approach to preventing or mitigating ransomware attacks.
HIT = health information technology.
Another approach to recover from a ransomware attack without needing to pay a ransom is by copying a file when it is being modified, storing one copy in a protected area, and allowing any changes to be made to the other [14]. ShieldFS© (NECSTLab, Milan, Italy) approaches this by creating a protected (i.e., read-only) copy of files when a process requests to modify or delete it [14]. If ShieldFS© determines that a process is malicious, the offending process is suspended and the copies can be restored, replacing the modified (encrypted) versions [14]. Conversely, Redemption uses a similar approach, but its technique creates a copy of each of the files targeted by the ransomware and then uses the Windows Kernel Development framework to redirect (or “reflect”) the write requests or filesystem operations (invoked by the ransomware to encrypt the target files) from the target files to the dummy copies in a transparent data buffer, hence leaving the original files intact [14].
\nLastly, any ransomware attack should immediately be reported to the appropriate authorities [37]. In the U.S., federal law dictates that any breach undergo a thorough and properly documented analysis to determine if any unsecured PHI was compromised [38, 39, 40]. For anything other than a low probability of PHI compromise, one must inform the U.S. Department of HHS as soon as possible, and no later than 60-days post-breach (when over 500 person’s PHI is affected) [10, 37, 41].
\nAs HIT infrastructure struggles with new technology and security protocols, the industry is a prime target for medical information theft. Even worse, the healthcare industry is lagging behind other leading industries in securing vital data. Healthcare organizations must adapt to the ever-changing cyber-security trends and threats, such as ransomware, where critical infrastructure is exploited, and valuable patient data are extracted. It is imperative that time and funding are invested in maintaining and ensuring the protection of healthcare technology and the confidentially of patient information from unauthorized access.
\nThe authors have no conflict of interests to disclose.
Proteins are chains of amino acids which are involved in nearly every process in the body. Proteins function as enzymes, transcription factors, binding proteins, transmembrane transporters and channels, hormones, receptors, structural proteins, and signaling proteins [1]. However, the primary role of protein in the diet is to provide amino acids required for the synthesis of new proteins. We especially rely on dietary protein to provide the nine essential amino acids, which cannot be synthesized in the body. Protein intake greater than the dietary recommendations may prevent sarcopenia [2], help maintain energy balance [3], improve bone health [4, 5, 6, 7] and cardiovascular function [8, 9, 10], and aid in wound healing [11]. This chapter focuses on the role of dietary protein, and the associated health benefits, throughout the life cycle.
\nThe current dietary recommendations for protein intake include the estimated average requirement (EAR) [12] and the recommended dietary allowance [12]. For daily protein intake, the EAR for dietary protein is 0.66 g kg−1 day−1, and the RDA is 0.8 g kg−1 day−1 for all adults over 18 years of age. This can become confusing when trying to make recommendations for individuals at different stages of life. Even the Food and Nutrition Board recognizes a difference between what is recommended in the RDA and the level of protein intake needed for optimal health [12]. Therefore, there is a third recommendation for protein called the acceptable daily macronutrient range (ADMR) [13, 14]. The ADMR includes a recommendation for protein intakes ranging from 10 to 35% of daily energy (e.g., calorie intake), which makes the ADMR easier to use when developing dietary recommendations for protein [12].
\nA majority of the adult population in the United States exceeds the minimum recommendations for protein intake [15]. The current dietary protein intake in the United States is approximately 82 g d−1 for men and 67 g d−1 for women [16]. \nTable 1\n details the current protein intake as percent of energy intake in the United States based on sex and age. A majority of dietary protein comes from animal protein (46%), followed by plant protein (30%), dairy (16%), and mixed foods (8%) [16]. There is increasing evidence indicating that consuming dietary protein at levels above the current RDA (0.8 g dietary protein kg body weight−1 day−1) may be beneficial for children, adults, older adults, and physically active individuals [17]. For example, protein intake above the RDA may help reduce the risk of chronic diseases such as obesity, cardiovascular disease, type 2 diabetes, osteoporosis, and sarcopenia [13, 17]. However, high protein intake without a subsequent decrease in carbohydrates attenuates the beneficial effects of dietary protein [18].
\nAge | \nTotal | \nMen | \nWomen | \n
---|---|---|---|
Protein | \n|||
20–44 years | \n15.7 | \n16.1 | \n15.3 | \n
45–64 years | \n15.8 | \n16.0 | \n15.7 | \n
65–74 years | \n16.3 | \n16.6 | \n16.1 | \n
75 years and older | \n15.7 | \n16.1 | \n15.3 | \n
Percentage macronutrient intake in the United States by sex and age [19].
Adequate dietary protein intake is essential to support cellular integrity, growth, and physical function. Although protein malnutrition is not prevalent in the United States, there is little research on optimal protein requirements for health benefits in children. Current EARs are based on the factorial method and the nitrogen balance technique. The factorial method incorporates the estimated nitrogen (protein) requirement plus the rate of protein deposition and an estimate of the efficiency of protein utilization [20] which is derived from adult dietary protein needs [12]. By using the indicator amino acid oxidation method in a group of healthy children 6–11 years old, it was found that the mean and population-safe (upper 95% CI) protein requirements were 1.3 and 1.55 g kg−1 day−1, respectively. This is higher than the 2005 DRI for protein (0.76 and 0.95 g kg−1 day−1, respectively) [12]. A similar study using the nitrogen balance technique also found that protein requirements in children in this age range are above current recommendations at 1.2 g kg−1 day−1 [21]. These higher estimated protein requirements in children seem to be in line with current protein consumption patterns in different pediatric age groups. For instance, children 2–3 years old are currently daily consuming ~3.6 g/kg of ideal body weight, children 4–8 years old are currently consuming ~2.6 g kg−1 ideal body weight−1, and children 9–13 years old are consuming ~1.6 g kg−1 ideal body weight−1 [15]; however, the optimal protein intake for children is still under debate [22]. There are racial/ethnic differences in protein consumption in children (2–18 years old). For example, non-Hispanic black children eat about 5% below, non-Hispanic white children eat about 3% below, Hispanic children eat about 2% below, and Asian children eat less than 1% below the EAR for protein [15].
\nAlthough the currently established recommendations for protein intake in children may be lower than the requirements, the effect of diets higher in protein (e.g., 30% of total energy intake) in children is unclear [22]. Several studies have alluded to the potential benefit of higher protein intake dietary practices. For instance, diets higher in protein with a low glycemic index can be protective against obesity in children aged 5–18 years [23], and diets higher in protein can lead to smaller waist circumference, blood pressure, insulin, and serum cholesterol than lower-protein diets in children from the same age group. A recent cohort analysis found that protein intake in 8-year-olds is associated with higher fat-free mass [24], and an additional cohort analysis found that at ages 11, 15, and 22 years, protein intake is inversely associated with early adulthood BMI. However, protein intake at 2 years was positively associated with BMI and lean mass at age 22 [25], suggesting there are conflicting results regarding the benefits of increased dietary protein in children.
\nPregnancy is a period of rapid tissue growth during a short period of time. Maternal tissues, including breast, uterine, and adipose tissues, blood volume, and extracellular fluids, account for the largest amount of protein accretion during pregnancy at 60%. The remaining 40% of protein accretion occurs within the amniotic fluid, fetus, and placenta [26, 27]. In fact, protein needs to increase soon after conception to support tissue growth and development, maintenance of maternal homeostasis, and lactation preparation [27, 28, 29]. These alterations occur in an exponential way and only in response to adequate total energy intake. This means that protein deposition does not significantly change in the first trimester compared to pre-pregnancy, but increases during the second trimester and significantly increases to the highest levels of protein deposition in the third trimester. This variable period of growth makes it difficult to define recommendations regarding protein requirements. Thus, although current recommendations suggest constant protein intake throughout the duration of pregnancy, pregnancy may actually require an increase in protein intake throughout gestation to support adequate growth, although further research is needed. There are several benefits of protein intake during pregnancy including adequate maternal weight gain within recommendations, lower early pregnancy BMI, and decreased postpartum weight [30].
\nAlthough the benefits of increased protein intake during pregnancy are apparent as stated above, protein requirements during pregnancy are difficult to measure. This is due to the involved nature of some of the techniques used to measure protein requirements. Therefore, the current dietary protein recommendations during pregnancy are based on factorial estimates of recommendations for healthy, nonpregnant populations. Pregnancy protein needs have been derived from the EAR and RDA for healthy, nonpregnant populations and are set to 0.88 g kg−1 day−1 (EAR) and 1.1 g kg−1 day−1 (RDA) [12]. However, newer studies found protein needs to be 1.2 g kg−1 day−1 at 11–20 weeks, increasing to 1.52 g kg−1 day−1 at 30–38 weeks [31]. Both nonpregnant women of childbearing age (20–44 years) and pregnant women consume at or above the current recommendations of protein intake [32, 33]. One study [31] found that pregnant women consume the same amount of protein in early pregnancy (1.44 ± 0.30 g kg−1 day−1) as they do in late pregnancy (1.47 ± 0.53 g kg−1 day−1), not taking fluid retention and changes in body composition into account. These findings support others that have noted little overall change in dietary protein patterns from early to late pregnancy [33]. Collectively, these findings demonstrate that pregnant women meet the recommendations for dietary protein intake. Improvements may potentially be made to increase dietary protein requirements as pregnancy progresses.
\nAn important factor to consider when incorporating protein into the diet is how the source of dietary protein (e.g., protein derived from animal or plant sources) affects nutrient intake, nutrient adequacy, and diet quality [13, 34, 35]. Proteins with differing amino acid profiles exhibit varied digestion and absorption rates [36, 37, 38], and amino acid profiles depend directly on the quality and quantity of the dietary protein [37]. For example, the digestion and absorption rates of fast- (e.g., whey) versus slow (e.g., casein)-digesting proteins need to be taken into consideration when developing protein recommendations. One study provided young, healthy subjects with either a whey protein meal (30 g) or a casein meal (43 g) (both contained the same amount of leucine [one of the BCAAs]) and measured whole-body protein synthesis. Researchers determined that the subjects consuming the whey (fast) protein meal had a high, rapid increase in plasma amino acids, while subjects consuming the casein (slow) protein meal had a prolonged plateau of EAA [39]. In addition, the chemical structure and the presence of anti-nutritional compounds such as phytic acid within the protein source can influence digestion and amino acid availability [40]. Compared to animal sources, plant proteins are shown to have a lower anabolic impact on muscle; however, the reduced ability to elicit anabolic effects can be overcome by increasing protein intake and increasing the content of leucine [41].
\nWhether or not the amino acid source is derived from the whole protein or a mixture of free amino acids can also influence the rate of muscle protein synthesis [42]. For example, when older subjects were given either an EAA mixture (15 g) or a whey protein supplement (13.6 g) after an overnight fast, subjects consuming the EAA mixture had higher mixed muscle fractional synthetic rate [42], which is often associated with increases in muscle mass. The differing response could be due to the differing leucine content between the supplements (EAA, 2.8 g leucine, and whey, 1.8 g leucine) or because the EAA supplement was composed of individual amino acids while the whey protein supplement was intact protein. These subtle differences could influence the rate of appearance of the amino acids into blood circulation and thus the protein synthetic response.
\nAnother potential confounder of the protein synthetic response of various proteins is the form or texture of the protein itself, such as ground beef versus a beef steak [43]. When, older men consumed 135 g of protein as either ground beef or as a beef steak, the amino acids from the ground beef appeared more rapidly in the circulation than the amino acids from the beef steak. Whole-body protein balance was higher after consumption of the ground beef versus the beef steak. However, 6 h after the beef meals, muscle protein synthesis was not different [43]. Nonetheless, these data support that the form of the protein that is being consumed impacts digestion, absorption, and the rate of appearance of amino acids into circulation [35].
\nThe timing of dietary protein intake has received ample attention in the past several decades. Adults typically consume the majority of their protein intake at dinner (38 g) versus breakfast (13 g) [44]. However, recent research suggests that ingestion of more than 30 g of protein in a test meal does not further stimulate the effect of dietary protein on muscle protein synthesis [45]. This had led to discussion related to optimal timing of protein intake. For example, distributing protein intake throughout the day, timing of protein around nighttime eating, and protein eating at breakfast are all areas of increased interest. In general, research covering these topics is performed in young, healthy populations, or aging populations, and very few, if any, studies have been conducted in children and pregnant women.
\nBreakfast is often recognized as the most important meal of the day [46, 47, 48]. However, there is debate as to what defines the ideal breakfast meal [47], in addition to a lack of strong evidence to define which nutrients should be represented at breakfast [47]. A recent commentary published by the American Academy of Nutrition and Dietetics suggests that protein-containing foods (e.g., eggs, lean meat, and low-fat dairy products) should be included in breakfast meals [47]. Literature supports diets higher in protein aid in the treatment of chronic, metabolic diseases such as obesity, type 2 diabetes, and heart disease and have been shown to increase EE, improve satiety, regulate glycemic control, and improve body composition (reviewed in [13, 14, 34, 49]).
\nEating protein at night and immediately before bedtime has received substantial attention in the past decade. Although past common knowledge would claim that eating before bed precipitates negative effects on health and body composition, more recent studies show that there may be many metabolic, health, and body composition-related benefits [50]. Much of the previous research claiming the negative effects of nighttime eating was performed in shift workers [51], populations with night eating syndrome, who consume ≥50% of daily calories after dinner [52], and epidemiological data [53]. Although some of the negative effects of nighttime eating in these populations may include high BMI and abdominal obesity [54]; increased triglyceride concentration, dyslipidemia, and impaired glucose tolerance [55]; impaired kidney function [56]; and increased carbohydrate oxidation and decreased fat oxidation [57], many other factors need to be taken into consideration. For example, these populations are awake during abnormal hours and report sleep disturbances [58, 59]. In fact, the duration of sleep is inversely related to BMI [60, 61]. These populations also consume significantly more carbohydrate, protein, and fat throughout the day. Nonetheless, it is clear that eating large amounts of energy in the evening hours, in particular when the energy is carbohydrate- and fat-laden, may not be beneficial for health and body composition outcomes.
\nHowever, much more evidence has shown that eating a small protein snack (~200 kcal) before bed may elicit significant benefits. Improved muscle protein recovery, muscle mass, and strength gains mediated by enhanced overnight and next-morning muscle protein synthesis have been shown to be enhanced with 40 g of casein protein supplementation in elderly [62] and recreationally active men [63]. These effects are particularly enhanced when this dietary practice is added to the practice of resistance exercise [63]. In addition, reported hunger is lower and satiety is higher, and resting energy expenditure is higher the following morning after a small protein snack compared to a noncaloric placebo [50, 62]. Chronically (4 weeks) there are also reports of decreased blood pressure, decreased arterial stiffness [64], and a greater decrease in body fat in overweight and obese women when consuming nighttime protein [65, 66]. Importantly, these benefits are accompanied by no significant alterations in overnight or next-morning lipolysis, fat oxidation, substrate utilization, or any blood markers in obese men or resistance-trained young women [67].
\nCurrent research demonstrates that even distribution of protein intake throughout the day is more effective at stimulating a 24-h protein synthesis compared to an uneven distribution [68, 69]. This is supported by data from a longitudinal study on nutrition and aging, which found that even distribution of daily protein intake across meals is independently associated with greater muscle strength and higher muscle mass in older adult, but is not associated with loss in muscle mass [70] or mobility [71] over 2–3 years. However, there are some studies that fail to confirm the importance of spreading protein intake out over the course of the day [71, 72]. Additional studies have compared pulse feeding (72% of daily protein at lunch) versus protein being evenly distributed over four daily meals in hospitalized older patients for 6 weeks [73, 74]. These studies found that pulse feeding of protein increased postprandial amino acid bioavailability [75] and increased lean mass [74] compared to spreading protein intake throughout the day. Taken together, the optimal timing and distribution of protein intake still need to be determined.
\nObesity is a major public health concern [76] and is associated with the development of metabolic diseases such as cardiovascular disease, nonalcoholic fatty liver disease, and type 2 diabetes mellitus in both children and adults [77, 78]. Obesity is defined as having a body mass index (BMI) (weight in kilograms divided by height in centimeters squared) greater than or equal to 30.0. In 2015–2016, the prevalence of obesity (\nTable 2\n) in the United States was 39.6 for adults and 18.4% for youth [76]. Obesity also impacts racial and ethnic groups differently. For example, non-Hispanic black and Hispanic adults and youth have higher rates of obesity compared to non-Hispanic white and Asian populations [79].
\nAge group (years) | \nTotal (percent) | \nBoys or men (percent) | \nGirls or women (percent) | \n
---|---|---|---|
Youth, 2–19 | \n18.5 | \n19.1 | \n17.8 | \n
Young children, 2–5 | \n13.9 | \n14.3 | \n13.5 | \n
Youth, 6–11 | \n18.4\n$\n\n | \n20.4\n$\n\n | \n16.3 | \n
Adolescents, 12–19 | \n20.6\n$\n\n | \n20.2 | \n20.9\n$\n\n | \n
Adults, 20+ | \n39.6 | \n37.9 | \n41.1 | \n
Young adults, 20–39 | \n35.7 | \n34.8 | \n36.5 | \n
Middle-aged adults, 40–59 | \n42.8\n*\n\n | \n40.8\n*\n\n | \n44.7\n*\n\n | \n
Older adults, 60+ | \n41.0 | \n38.5 | \n43.1 | \n
Prevalence of obesity in the United States by age group and sex [76].
Significantly different from young children.
Significantly different from young adults.
A primary factor in controlling and preventing obesity and associated chronic diseases is through diet, for example, diets higher in protein [13, 14, 80, 81]. Diets higher in protein (>30% of energy intake) have been shown to improve body composition [82], improve glycemic response [81, 83, 84, 85], increase satiety [85, 86, 87], and increase postprandial energy metabolism [88, 89], which are all mediating factors of weight loss.
\nSarcopenia is the term for age-associated loss of muscle mass and function [35]. The loss of muscle function associated with sarcopenia is often referred to as dynapenia [90]. A loss or reduction in skeletal muscle function often leads to increased morbidity and mortality either directly, or indirectly, via the development of secondary diseases such as diabetes, obesity, and cardiovascular disease [91]. The causes of sarcopenia include poor nutrition, diminished responsiveness to anabolic hormones and/or nutrients, and a sedentary lifestyle.
\nThe loss in muscle mass observed with aging is often accompanied by an increase in fat mass [92], which can happen even in the absence of changes in BMI [35]. The loss in muscle mass results in a decrease in basal metabolic rate (BMR) or the amount of caloric energy we use while at rest [93]. The loss of muscle mass induces a 2–3% decrease in BMR per decade after the age of 20 and a 4% decline in BMR per decade after the age of 50 [93, 94]. Muscle loss and subsequent reduction in metabolic rate contribute to obesity that accompanies the aging process.
\nSeveral studies identify protein as a key nutrient for aging adults [2, 95]. Low protein intake is linked to a decrease in physical ability in aging adults [96]. However, protein intake greater than the dietary guidelines may prevent sarcopenia [96], help maintain BMR [3], improve bone health [4, 5, 6, 7], and improve cardiovascular function [8, 9, 10]. These benefits of increasing protein in the diet may improve function and quality of life in healthy older adults, as well as improve the ability of older patients to recover from disease and trauma [91].
\nCurrently, the dietary recommendations for protein intake are the same for all healthy adults above the age of 19. However, experts in the field of protein and aging recommend a protein intake between 1.2 and 2.0 g kg−1 day−1 or higher for elderly adults [91, 95, 97]. The RDA of 0.8 g kg−1 day−1 is well below these recommendations and reflects a value at the lowest end of the AMDR. It is estimated that 38% of adult men and 41% of adult women have dietary protein intakes below the RDA [16, 44].
\nBoth protein amount and source are important to consider when recommending protein intake to older adults [34, 35]. There are three important aspects to take into consideration when recommending a protein source: (1) the characteristics of the specific protein, such as the amount of essential amino acids (EAA); (2) the food matrix in which the protein is consumed, for example, as part of a beverage or a complete meal; and (3) the characteristics of the individuals consuming the food, including health status, physiological status, and energy balance [34]. In addition, the difference in digestibility and bioavailability of a protein can impact the quantity of protein that needs to be ingested to meet metabolic needs; this is especially important in older adults since gastric motility and nutrient absorption decrease with age. The speed of protein digestion and absorption of amino acids from the gut can influence whole-body protein building [36]. Proteins with differing amino acid profiles exhibit different digestion and absorption rates [36, 38, 98]. Amino acid availability depends directly on both the quality and quantity of the dietary protein [98].
\nOver the past 15 years, the gut microbiome has received increased attention regarding its role in impacting overall health [99]. Interestingly, it has been shown to influence diseases associated with metabolic health [100]. The intestinal mucosa houses nearly a trillion microorganisms, and the plasticity of this environment is highly reactive to changes in diet [101]. For instance, the gut becomes an active site for protein and amino acid metabolism prior to absorption. Following enzymatic denaturation by intestinal proteases, amino acids can become fermented into various metabolites which include short-chain fatty acids and ammonia [102]. The acute microbial response and long-term adaptation associated with dietary habits have become an important area of research.
\nAs gut assay methodologies improve, researchers have identified associations between microbial populations and their metabolite concentrations in response to dietary patterns. For instance, in vitro and human models demonstrate a potential negative link between animal protein intake and protein fermentation end products such as ammonia and trimethylamine-N-oxide [103, 104]. However, favorable outcomes associated with animal- and plant-based protein sources have been observed. For example, ingestion of both whey [105] and pea protein [106] has been shown to increase favorable gut bacterial species such as Bifidobacterium. In addition, supplementation with pea protein intake has been shown to increase the production of short-chain fatty acids, an important energy substrate utilized by enterocytes [106].
\nThere is sufficient evidence that protein intake higher than the current dietary recommendations is beneficial for most healthy individuals throughout the life cycle. However, benefits of dietary protein depend on the quality, the quantity, and the timing of protein intake. Although health benefits of dietary protein have been well-established for older adults, more research is needed to determine the health benefits of increased dietary protein intake through each state of life.
\nThis work was supported by a grant to J.I.B. and E.B. from the Arkansas Biosciences Institute.
\nThe authors have no conflicts of interest to declare.
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