The benefits of exercise to a Down’s Syndrome population

Viviane Merzbach (UK) and Dan Gordon (UK)

Sport and Exercise Science Research Group, Anglia Ruskin University, East Road, Cambridge, CB1 1PT

Abstract

The benefits of exercise and training for a reference population are well understood and the merits well documented.  The aim of this review is to ascertain the benefits of exercise for a Down’s Syndrome population.

There is controversy on physical activity levels in people with Down’s Syndrome; most studies report a highly sedentary lifestyle for those individuals where physical activity recommendations are not met whilst others find no difference in activity levels between siblings with and without Down’s Syndrome. However, most individuals with Down’s Syndrome have to overcome social and environmental barriers to physical activity. The physiological characteristics of the Down’s Syndrome individual exhibit potential limitations and restrictions to both cardiovascular and resistance based exercise, with poor skeletal muscle development and chronotropic incompetence being the primary constraints.  The merits to the Down’s Syndrome individual are clear with many being classed as obese and showing classic signs of the contraindications to exercise.

There is limited data available as to the physiological responses to exercise and training, but those presented highlight both benefits in terms of the physiological responses and inconsistencies in terms of methods applied.  The physiological responses in terms of cardiovascular and bi-motor abilities are explored and examined showing that a key stimulus for adaptation are the ground impact forces (GIF).  An overriding factor that affects all of the presented outcomes is the adherence of the individual to the program, with dropout rates greater than 50% in six months being reported.

The conclusion would appear to be that a program is developed which is structured, and stimulating and conforms to the needs of the Down’s Syndrome individual, taking into account their specific physiological needs.

Key words:  Down’s Syndrome, exercise, physiological adaptation, adherence

Introduction

In the population as a whole the benefits of regular exercise have been well researched and established Astrand et al (2003).  Indeed it has been documented that regular aerobic (cardiovascular) exercise induces physiological responses which are of profound significance to the health of the individual Blair et al (1999); Fletcher et al (1996); American College of Sports Medicine (1998).  Of these adaptations perhaps the most pertinent are an increased functioning and efficiency of the myocardium, decreased cholesterol levels, decreased systolic and diastolic blood pressure at rest and during exercise, decreased adipose tissue stores and the concomitant result in a decreased prevalence of the contraindications to health such as diabetes mellitus and coronary heart disease Fletcher et al (1996).

Yet despite the widespread interest to the clear benefits of exercise per se on health and lifestyle there is a paucity of suitably applicable information for individuals with intellectual disabilities. This should be considered to be both surprising and concerning, given that individuals with less education, lower incomes, and blue collar employment are more likely to be physically inactive than those with more education, higher incomes and white collar employment Crespo et al (1999).  Individuals with an intellectual disability, represent a population group who fit into the low education, low income blue collar worker group Braddock et al (1999); Fujiura et al (1998), and these individuals have been shown to be less physically active when compared to age matched individuals Beange et al (1995).

In a group of participants with intellectual disabilities with and without Down’s Syndrome, males are significantly more active than females and physical activity levels are decreased in individuals with Down’s Syndrome when compared to participants without Down’s Syndrome as shown in table 1. However, no participant irrespective of age and severity of intellectual disability met the current UK physical activity recommendations Phillips et al (2011). In contrast to the study by Phillips et al (2011), Whitt-Glover et al (2006) demonstrated in their group of siblings (at least one child with Down’s Syndrome and one sibling without any disabilities) that almost all of the participants exceeded the guidelines set for children to achieve at least 30 minutes of moderate physical activity daily. Surprisingly, there were no significant differences found for inactivity, low physical activity and moderate physical activity levels between children with Down’s Syndrome and their unaffected siblings, only the amount of vigorous physical activity was higher in the children without Down’s Syndrome. In general, the literature agrees that physical activity levels depend on the severity of the intellectual disability. Lower levels of impairment are correlated with higher participation in physical activity whilst individuals with severe intellectual disability show a more sedentary lifestyle Frey et al (2008); Bartlo et al (2011).

Table1

Based on 152 participants aged 12-70 years with mild to severe levels of ID from south-east and east of UK.
MVPA= moderate to vigorous physical activity, Wear time= wear time of accelerometer, IDnoDS= intellectual disability without Down’s syndrome, DS= Down’s syndrome, *= significant difference between males and females or IDnoDS and DS
Reference: Phillips AC, Holland AJ (2011)

People with Down’s Syndrome are facing complex problems and a vast variety of barriers that prevent them from participating in physical activities. Several authors Whitt-Glover et al (2006); Johnson (2009); Bartlo et al (2011); Pett et al (2013); Shields et al (2013) and in detail Bodde et al (2009) highlight the difficulties for people with intellectual disabilities with and without Down’s Syndrome to overcome social and environmental barriers and engage in physical activity. The key barriers outlined are lack of money, transportation, access and support from family and carers. It has to be highlighted that parents and caregivers need to change their perception of individuals with Down’s Syndrome being too fragile to participate in exercise and especially vigorous physical activity and provide encouragement rather than negative support (comments such as “Be careful” and “Don’t overdo it”) Whitt-Glover et al (2006); Bodde et al (2009). In most cases, people with Down’s Syndrome prefer to exercise with someone; however, suitable programmes with appropriately trained staff are limited. For these reasons, it is challenging for people with intellectual disability to improve their overall physical health and well-being through physical activity.

The study by Pastore et al (2000) demonstrated that from a cohort of 42 individuals with Down’s Syndrome, 43% were classed as obese, 20% had reduced Forced Vital Capacity (FVC) scores, 61% of the group showed low exercise tolerance, which appeared to be associated with 91% of the cohort displaying mild tachycardia.  All of these factors indicate poor cardiovascular health and functioning which according to Heller et al (2004) are associated with poor self efficacy and decreased life satisfaction.

Therefore the purpose of this paper is to review the literature available on exercise for individuals with intellectual disabilities and propose recommendations for interventions in terms of regimes for developing health and fitness.

Physiological characteristics

Individuals with intellectual disabilities have low levels of work capacity and peak oxygen consumption (VO₂max); Guerra et al (2003) and these levels are further exacerbated in individuals with Down’s Syndrome, as presented in table 2 Wee et al (2015). Adolescents and young adults with Down’s Syndrome have comparable reduced aerobic capacities as seen in old adults (60 years-old) without disabilities but with heart disease Baynard et al (2008); Cowley et al (2010).

Table 2

Measures of BMI and cardiovascular fitness in individuals with Down’s syndrome (DS), intellectual disabilities without Down’s syndrome (IDnoDS) and without intellectual disabilities (NoID).
BMI (body mass index) kg∙m², peak HR (peak heart rate) b∙min^-1, VO₂peak (peak oxygen uptake) ml∙kg^-1∙min^-1. The data was not influenced by gender of the participants.
Reference: Wee SO, Pitetti KH, Goulopoulou S, Collier SR, Guerra M, Baynard T (2015)

It is reasonably well established in the population as a whole that peak oxygen consumption (VO₂max) is limited by a combination of both central and peripheral mechanisms; Bassett and Howley (2000). This being the case it is not surprising that Down’s Syndrome individuals exhibit low aerobic fitness scores primarily as a result of a reduced red blood cell count Monterio et al (1997) and in many cases chronotropic incompetence Baynard et al (2004); Fernhall et al (2001); Guerra et al (2003). As a result there is a reduced cardiac output and oxygen carrying capacity therefore impairing the ability of the individual to exercise aerobically, with a potential consequent effect on daily functioning Fernhall et al (2001).

Chronotropic incompetence has been attributed to alterations in autonomic cardiac control, and therefore altered autonomic function Fernhall et al (2003); Fernhall et al (2001), the significance of which is that alterations in autonomic cardiac control are associated with increased risk of early mortality and morbidity Pomeranz et al (1985); Huikuri et al (1999). Interestingly it has been reported that obesity has been related to altered autonomic function Matsumoto et al (1999), further highlighting the need to develop aerobic functioning and overall fitness in the Down’s Syndrome population. However, Wee et al (2015) found that body mass index (BMI) in adults with Down’s Syndrome does not strongly affect maximal oxygen consumption (VO₂max) and has no effect on VO₂max in children/adolescents. They suggest that chromosomal abnormalities have stronger effects on autonomic function rather than the effect of overweight/obesity. Further, they propose that the already very low aerobic reserve of children with Down’s Syndrome is not hugely affected by aging and therefore obesity is not playing a main role in the reduced aerobic capacity in older individuals with Down’s Syndrome. This is the contrary in individuals with an intellectual disability without Down’s Syndrome and healthy persons where being overweight/obese is linked to a reduced VO₂max.

In a reference population (Rpop) it has been established that there is a relationship between aerobic fitness and bone mineral density Kronhead et al (1998), with the association suggesting that in those individuals who undertake regular exercise there are higher bone mineral density (BMD) scores and a decrease in the value is associated with decreased levels of loading on the musculoskeletal system Heinonen et al (1999).  Further it has been suggested that in both recreational runners/joggers and elite athletes where there are increased levels of ground impact forces (GIF) and hence loadings on the lower limbs when compared to sedentary individuals there is an attenuated decline in bone mineral density with age Noakes (1991).

In the Down’s Syndrome population there is good evidence to show that there are both reduced bone mineral density and lower limb strength scores when compared to both age matched able bodied and individuals with an intellectual disability without Down’s Syndrome, Angelopoulou et al (2000).  Indeed Angelopoulou et al (2000) demonstrated that bone mineral density was 26% lower in Down’s Syndrome compared to their matched able bodied counterparts. They also demonstrated significantly reduced muscular strength across a range of angles 300º - 60º in the quadriceps and hamstring groups when compared to both a reference population (Rpop) and individuals without Down’s Syndrome  (p< 0.05).  These findings are supported by both Horvat et al (1997) and Croce et al (1994) who showed that in Down’s Syndrome individuals there were reduced peak torque and average power scores when compared to individuals without Down’s Syndrome and the reference population (Rpop).  There are clear implications from these findings for health and fitness within a Down’s Syndrome population.  As has already been highlighted individuals with intellectual disabilities are less likely to exercise and hence are potentially exacerbate the already low bone mineral density scores, the implications of which are early onset of osteoporosis and brittle bones Kronhead et al (1998).

Poor muscular strength especially in the lower limbs has been associated with increased neuromuscular recruitment of synergistic muscles Hakkinen et al (1985). The subsequent effect during exercise would be an increased oxygen cost per muscle contraction resulting in premature onset of fatigue.  In the study by Cowley et al (2010) knee extensor strength, as a critical factor of functional skills in people with Down’s Syndrome, was found to be a good predictor of timed performance in tasks of daily living such as walking upstairs and downstairs and rising from a chair. The oxygen cost for these tasks is increased in individuals affected by Down’s Syndrome. Particularly upright locomotion is influenced by muscle hypotonia and joint laxity which result in slow walking velocities, shorter steps and wider strides and an overall gait instability for people with Down’s Syndrome throughout their lifespan Mendonca (2009); Mendonca (2010); Sukriti et al (2011). As such the implications for an exercise regime in Down’s Syndrome individuals would appear to be established both from a physiological and social context.

Physiological responses to exercise

As has already been highlighted there is a paucity of available data on the physiological characteristics let alone on the responses to training to Down’s Syndrome individuals and those without Down’s Syndrome. The data available is presented in tables 3 and 4 showing the cardiovascular and neuromuscular responses to training in both Down’s syndrome and non-Down’s Syndrome individuals.  Rimmer et al (2004), Tsimaras et al (2003) and Mendonca (2009) demonstrated increases in cardiovascular function (P< 0.05), whereas the other studies cited show no change in this and associated factors.

Table 3

• Cardiovascular responses to training
• denotes increase, ¯ denotes decrease, « denotes no change
• CV= Cardiovascular St= Strength, Wt= Weight (mass), LE= Locomotor economy, VO₂max= Maximal aerobic power,
• VE= Minute ventilation, RER= respiratory exchange ratio, Tlim= Time Limit to exhaustion, RBC= Red Blood Cell Count,
• HDL= High density Lipoprotein, VLDL= Very Low Density Lipoprotein

limited in terms of scope a number of conclusions/inferences can be drawn from these studies. Data from the reference population (Rpop) suggested that in order to develop aerobic/cardiovascular adaptations takes in the region of 12 weeks Kubukeli et al (2002), with minimum responses occurring in around eight weeks Jones and Carter (2000). Interestingly both Rimmer et al (2004), Tsimaras et al (2003) demonstrate significant increases in cardiovascular function following a twelve-week period of sustained exercise and the 28-week programme in Mendonca et al (2009) study did elicit a 27.8% increase in peak aerobic power and a 30.1% improvement in peak pulmonary ventilation. Yet Varela et al (2000) demonstrated no change in cardiovascular function following a 16-week period of exercise. This disparity could be addressed by examining the exercise modality in use. Rimmer, Tsimaras and Mendonca used weight bearing exercise such as jogging, walking and stepping, while Varela used rowing on an indoor rowing ergometer.  There are clearly different physiological responses to these forms of exercise, with rowing being associated with more rest per action than either jogging or walking. Indeed (Astrand et al 2000) demonstrated that during rowing the rest to work ratio is in the region of 2:1, whereas for running it is 1:1. The implications of this would be that the individual would encounter less fatigue during the rowing than walking and hence would elicit lower physiological responses and less cardiovascular adaptation.

The benefits of weight bearing exercise have been well documented with a principal peripheral stimulus to cardiovascular exercise being the number of impact forces registered by the musculoskeletal system Kubukeli et al (2002). Indeed Ulrich et al (2001) demonstrated that in a group of infants 307.4±58.9 days, where treadmill walking was actively encouraged there was a significant difference in the onset of independent walking when compared to controls (73.8 and 101 days respectively).  The implication of this is that the initiation of independent walking is dependent upon the development of specific movement patterns and the consequent improvement and integration of functional motor responses Badke et al (1990). These findings have significance to the wider issue of exercise and health as the development of motor function and co-ordination have been associated with enhanced oxygen consumption and muscular efficiency Jones and Carter (2000).

A criterion measure of health is the enhanced ability to consume and utilise oxygen, primarily as a result of specific key physiological adaptations such as increased myocardial functioning Bassett and Howley (1995), increased oxidative enzymes Kubukeli et al (2002), increased slow twitch muscle fibres Jones and Carter (2000) and increased red blood cell count Noakes (1991). The latter is an interesting point given that Monteiro et al (1997) demonstrated a non significant change in red blood cell count (RBC) following a 16 week period of aerobic exercise.

A possible reason for the disparity in the results may be associated with the intensity, frequency and duration of the exercise bouts. The physiological adaptations previously highlighted are dependent on the interplay between these three factors, i.e. how hard an individual trains (intensity), how often they train (frequency) and how long they train for (duration). The combination of these factors is described as training volume Bompa (1999). In most studies exercise intensity is either classed as a percentage of maximal oxygen consumption (VO₂max) or a percentage of maximum heart rate (HRmax). The merits of using these as criterion measures are discussed elsewhere Astrand et al (2003) but their use for Down’s Syndrome and non-Down’s Syndrome are less well understood.

The limitations to using heart rate as a measure of exercise intensity in a Down’s Syndrome population were analysed by Fernhall et al (2001) who suggested that Down’s Syndrome individuals exhibit a 20-25% lower maximal heart rate when compared to the reference population and that individuals without Down’s Syndrome demonstrate an 8-12% reduced maximal heart rate when compared to the reference population. As a result it is perhaps not surprising that the standard method for determining maximal heart rate (220-age) significantly over predicts maximal heart rate, even though in a reference population this formula provides a conservative estimate. Indeed Robergs (2003) demonstrated that there is no scientific rationale behind the concept of 220-age and as such the use of this method should be viewed with some caution. Therefore it is possible that Millar et al (1999) when using heart rate as a measure of exercise intensity under-predicted the exercise intensity and as a result the participants experienced less fatigue inducing stimulation and hence developed less physiological adaptation (p<0.05). As such Fernhall et al (2001) have proposed the use of a new nomogram/equation for the calculation of maximal heart rate, but still recommend caution when using what is in essence an unreliable variable for determining exercise intensities, especially those in excess of the metabolic threshold Cooper (2001).

The fact that Monterio et al (1997) demonstrated non significant changes (p< 0.05) in aerobic parameters could also be explained by the choice/use of baseline measure from which exercise intensity was determined. Reviews Gordon (2015); Astrand (2000); Bassett and Howley (1995) have suggested that less than 50% of all subjects exhibit a maximal effort during a maximal oxygen consumption (VO₂max) test. Termination of exercise has been associated with both central and peripheral factors including lack of motivation and the onset of pain, thereby producing oxygen consumption (VO₂) values that could not be classified as maximal but rather a peak, thereby indicating that ‘more’ physiological reserve could have been tapped into. This trend for stoicism during stress testing is magnified in both Down’s Syndrome and non-Down’s Syndrome individuals primarily as a result of intellectual capacity and reduced motivation for what is a complex task. However, Mendonca et al (2010) are suggesting a true physiological limitation as reason for a reduced exercise capacity in Down’s Syndrome; they pointed out that peak exercise testing in participants with Down’s Syndrome was reliable and repeated test values were in the range of those for individuals without intellectual disabilities. This result needs to be interpreted with caution because it is based on a small group of people with Down’s Syndrome and also the severity of intellectual disability plays an important role in peak exercise testing.

It is well established that maximal oxygen consumption is dependent on cardiac output (Q) and hence the incidence of chronotropic incompetence within the Down’s Syndrome population would exacerbate the poor maximal oxygen consumption (VO₂max) scores evident in this group. There is strong evidence in supporting this hypothesis that chronotropic incompetence is one of the main causes for the reduced aerobic power in persons with Down’s Syndrome. Participants with Down’s Syndrome showed chronotropic response index values that are comparable to non-disabled individuals with true chronotropic incompetence. This submaximal exercise variable is independent of effort, motivation, age, resting heart rate, and physical fitness Mendonca et al (2010). The consequent effects of low VO₂max scores would be evident in the calculation of the exercise intensity (%VO₂max).  If the VO₂max score is not truly maximal then the submaximal exercise intensities would be misinterpreted and as with the heart rate calculations the subsequent physiological adaptations would be less evident.

Despite the issues surrounding the interpretation of the results from some of the studies there is good reason to support the use of an exercise programme for individuals with Down’s Syndrome.  Wang (2003; 1997) demonstrated that repeated jumping exercise enhanced bi-motor abilities in both Down’s Syndrome and non-Down’s Syndrome individuals, when performed over a six-week period.  The fact that the group only reported bi-motor responses may suggest a limited applicability. However we can, though, make some inferences from these and previous studies.

Table 4

Neuromuscular responses to training

­

denotes increase, ¯ denotes decrease, « denotes no change

PRT= Progressive Resistance Training, VR= Virtual Reality (Wii console), Bal= Balance

St= Strength, UL= Upper Limb, LL= Lower Limb, Wt= Weight (mass), End= Endurance, Func= Function, Sp= Speed, PT= Peak Torque, dBA= dynamic Balance Ability, FWk= Floor walk, BWK= Beam walk, VJ= Vertical Jump, HJ= Horizontal jump, Fsd= Floor standing, Bsd= Beam standing AgA= Agonist activation, PV= Peak Velocity, Acc= Acceleration, Dec= Deceleration, AntA= Antagonist activation

As has previously been highlighted, most aerobic exercise involves ground impact forces (GIF) and the associated metabolic costs involved with this activity.  Therefore it is highly likely that in these two studies, Wang et al would have demonstrated improvements in relation to aerobic parameters in conjunction with the gains in bi-motor abilities. This form of activity clearly meets the needs of an exercise regime in that it would enhance cardiovascular fitness, develop bi-motor abilities and would not be subject to intellectual difficulties associated with more complex tasks.

There are still issues surrounding impact activity on joint stability especially when there is associated muscle instability and skeletal muscle weakness as evidenced in a Down’s Syndrome population. Despite these potential limitations the findings of Wang offer considerable benefits to the exercising Down’s Syndrome individual. The results indicated increased ability at skilled movements such as a beam walk and floor heel-to-toe walk. These improvements highlight increased muscle tone and postural control (Wang et al 2003) which are of pronounced benefit to the individual in terms of health and lifestyle.

Furthermore, significant improvements in upper and lower limb muscle strength were reported after six-week to ten-week programmes using different training modalities such as progressive resistance training, agility, balance and jump training Shields et al (2008); Sukriti et al (2011); Lin et al (2012) and Shields et al (2013). The improvements in muscle strength in these relatively short interventions point towards increases in neural recruitment which can be seen after four to eight weeks of training.

Of interest is the time course of adaptations for skeletal muscle to imposed loading (resistance). In a reference population (Rpop) it has been demonstrated that the time course for these adaptations is phased. The initial response, ~6 weeks is an increased strength of the engaged muscles, but without any significant hypertrophy Sale (1988).  This paradoxical response has been explained Hakkinen (1985) by an enhanced neural recruitment response. Therefore it appears that the increased strength in this initial phase is a result of an enhanced ability to recruit engaged muscle fibres more rapidly and in greater numbers, rather than from increases in muscle mass Sale (1988).

The development of muscle hypertrophy has been shown to be statistically significant after 12 weeks Sale (1988); Hakkinen (1985). At this point the neural recruitment is slightly diminished but greater than at the onset of the exercise regime.

The fact that Wang (2003; 1997) and Almeida (1991) demonstrated enhanced bi-motor abilities after 2-6 weeks would be evidence of neural adaptations rather than changes in the contractile structures. What is not clear to date is whether these adaptations follow the same time course in the Down’s Syndrome individual when compared to the reference population. Again despite this limitation the evidence is good for an enhanced ability following a period of training.

An issue that links all exercise programs and is evident in both the reference population and Down’s Syndrome population is adherence to the task. There is compelling evidence Martinsen (1993) that in a reference population 50% of participants will drop out of an exercise program within the first six months. It has been observed that this drop-out rate is higher for aerobic based work than those which are less aerobic and that there is little difference between clinical and non-clinical populations Robinson and Rogers (1994). What is well understood is that when individuals participate in a structured exercise program the drop-out rate can decrease to as little as 10-15% Martin and Dubbert (1985); Robinson and Rogers (1994). In the study by Pett et al (2013) the attendance rate for a 24-session intervention was over 70%; the intervention focussed on healthy lifestyle changes in overweight and obese young adults with intellectual disabilities through health education and physical activity sessions. In this context what should not be underestimated is that the exercise should be enjoyable and appealing to the individual, indeed this is considered a primary reason for the high dropout rates previously stated Wankel (1993). The attendance rates for two different strength training programmes using progressive resistance training was 92%. The first study used a group-based programme with the participants exercising together Shields et al (2008) and the second study introduced a student-led intervention where a 3-month follow-up assessment showed that only 3 out of 34 participants dropped out post intervention whilst the remaining participants maintained their level of physical activity 24 weeks post intervention Shields et al (2013). Lin et al (2012) presented a highly enjoyable programme which was a combination of treadmill exercise and the use of a Wii game console with a Wii sports collection. The attendance rate for the 18 treatment sessions was 100% and the six-week programme led to a decrease in body weight and an increase in muscle strength and agility. At present there is very little data highlighting adherence in either the Down’s Syndrome or non-Down’s Syndrome population although it is perhaps worth noting that both Peran (1997) and Eberhard et al (1997) demonstrated significant cardiovascular and health adaptations following completion of a supervised adapted program. But more research is needed that uses follow-up assessments after the intervention programmes.

Conclusions

The consensus is that exercise is of clear benefit to the Down’s Syndrome individual both in terms of cardiovascular and neuromuscular responses. In a wider sense, basic function and vocational performance is positively affected by exercise; improvements in adaptive skills will make people with Down’s Syndrome more independent in leisure and work opportunities Mendonca et al (2010). The exercise task initiated needs to be simplistic in nature but at the same time sufficient in terms of the imposed demand placed on the body. Wang et al (1997); (2001) demonstrated benefits from performing jumping exercise although there are considerable limitations to a long term exercise program involving a single activity. As such a recommendation would be to introduce a programme that offers diversity and interest while at the same time avoiding tasks that are either perceived as being complicated or that are directly associated with being classed as exercise. A good example for a highly enjoyable programme is the one by Lin et al (2012) who used a combination of walking/jogging and virtual reality Wii game console exercise. Shields et al (2008); (2013) introduced two different options of programming exercise interventions for people with Down’s syndrome. They used either a group-based training where two to three individuals with Down’s Syndrome exercised together with one supervisor present or they introduced a programme which was led by student mentors. This form of ‘training’ can then stimulate social interaction as well as physiological adaptation and avoids many of the pitfalls associated with prescribed exercise programs Millar et al (1993); Monteiro et al (1997); Varela et al (2001). As previously mentioned, certain barriers to physical activity are evident for people with Down’s Syndrome and therefore exercise programmes have to be cost efficient and motivating which can be seen by a 92% attendance rate in the programmes by Shields et al (2008); (2013) and 100% adherence in Lin et al (2012).

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This article was written especially for the website. It was originally published in May 2006 and revised in March 2015.