HI

Heart International 2016; 11(1): e32-e40

DOI: 10.5301/heartint.5000232

eISSN 2036-2579 REVIEW

Influence diagram of physiological and environmental

factors affecting heart rate variability: an extended
literature overview
Julien Fatisson1, Victor Oswald1,2, François Lalonde1,3
1
Association of Research in Osteopathy in Quebec (AQRO), Montreal - Canada
2
Department of Neurosciences, Faculty of Medicine, University of Montreal (UdeM), Montreal - Canada
3
Departement of Physical Activity, Faculty of Sciences, University of Quebec in Montreal (UQÀM), Montreal - Canada

ABSTRACT
Heart rate variability (HRV) corresponds to the adaptation of the heart to any stimulus. In fact, among the pa-
thologies affecting HRV the most, there are the cardiovascular diseases and depressive disorders, which are as-
sociated with high medical cost in Western societies. Consequently, HRV is now widely used as an index of health.
In order to better understand how this adaptation takes place, it is necessary to examine which factors directly
influence HRV, whether they have a physiological or environmental origin. The primary objective of this research
is therefore to conduct a literature review in order to get a comprehensive overview of the subject.
The system of these factors affecting HRV can be divided into the following five categories: physiological and
pathological factors, environmental factors, lifestyle factors, non-modifiable factors and effects. The direct in-
terrelationships between these factors and HRV can be regrouped into an influence diagram. This diagram can
therefore serve as a basis to improve daily clinical practice as well as help design even more precise research
protocols.
Keywords: Cardiac coherence, Heart rate variability, Influence diagram, Literature overview

Introduction This adaptation is called heart rate variability (HRV) and can
also be characterized in terms of amplitude: weak, normal or
“Life is about rhythm. We vibrate, our hearts are pump- high. A high HRV is the sign that the heart is healthy since it has
ing blood, we are a rhythm machine, that’s what we are.” - more flexibility to react to any stress (physiological or environ-
Mickey Hart. With its strategic position, the heart acts not mental). Alternatively, a reduced HRV is a symptom of health
only as the main pump but also as a global coordinator in problems and can affect immune functions, self-regulation
synchronism with the other body functions. Because of the and psychosocial abilities (1). Among the pathologies affecting
influence of many factors, the heart does not maintain the HRV the most, there are the cardiovascular diseases (CVD) and
exact same rhythm from one heartbeat to the next. It reacts depressive disorders.
to any stimulus by increasing or decreasing its rhythm so that One can therefore wonder what kind of factors can di-
the body can adapt to any change. rectly influence HRV. Actually, many specific reviews already
focused on HRV in order to described in precise details
how specific brain areas are affecting HRV, how heart dys-
functions can influence individual health, how respiration
Accepted: July 8, 2016
induces heart acceleration or deceleration, how stress fac-
Published online: September 15, 2016
tors act on the heart, and so on. There were very numerous
studies, such that HRV is now commonly used as a health
Corresponding author:
Julien Fatisson indicator.
Association Québécoise de Recherche en Ostéopathie (AQRO) Despite all of these numerous studies and reviews, none
Département de l’activité physique was carried out to regroup all the information. The original-
Faculté des sciences ity of this literature review is to analyze the numerous previ-
UQÀM, Complexe des Sciences ous reviews and meta-analyses in order to present an over-
Pavillon des sciences biologiques (SB) view of the problem, to create a comprehensive map of the
Local: SB-4630
141, Avenue du Président Kennedy
main factors influencing HRV. Knowing all the environmental
Montréal, Québec and physiological factors and how they can influence amongst
H2X 1Y4, Canada themselves will help to build more precise research protocols
[Link]@[Link] and also help clinicians in their daily practice for treatment

© 2016 The Authors. This article is published by Wichtig Publishing and licensed under Creative Commons Attribution-NonCommercial-NoDerivatives 4.0
International (CC BY-NC-ND 4.0). Any commercial use is not permitted and is subject to Publisher’s permissions. Full information is available at [Link]
Fatisson et al e33

and recommendations to their patients. Actually, with the

specific methodology described below, the categorization
phases of this study could point out five main themes among
the counted elements: physiological and pathological factors,
lifestyle factors, non-modifiable factors, neuropsychological Fig. 1 - Schematization of the method used for the creation of a
diagram of influence towards heart-rate variability (HRV).
factors and environmental factors. These categories will be de-
tailed and a synthesis of the links between them will be further
presented with a diagram of influences. (source), a transfer towards the target (exposure) or
a harmful effect (target). In the influence diagram, a
Methods cause is connected to an effect by a single-direction
arrow. Some elements could not be assimilated to a
This literature review was carried out according to a system- cause or an effect since they could be both. In this
atic protocol, commonly used (2, 3). With search tools such as case, double direction arrows are to be used.
PubMed, Medline, and Scopus, the literature search was con- • Second, all the identified elements were regrouped
ducted in summer 2015 with the following keywords in com- into five different specific categories, detailed fur-
bination: heart rate, coherence, variability, physiology, heart ther in the Results section.
brain connection, electromagnetic field, blood pressure, cere- - Step 3: Establish the nature of cause to effect links (ben-
bral, emotions, neurocardiology. Several scientific validity crite- eficial, harmful or undefined) between the identified el-
ria were verified for each original article: presence of controls, ements and HRV. Different types of arrows were used in
randomization, statistical analysis, and results’ ­significance. the diagram to account for this aspect. Details are given
Systematic review articles as well as meta-analyses in the figure legend.
were first consulted. References in these articles were then - Step 4: All data and observations during this step were then
consulted in order to identify additional studies. Following compiled and structured for all elements, as well as for the
this step, in order to refine the results, a descending meth- links uniting them, in the form of an influence diagram (step
od was used from recent secondary sources. In front of the 4), by using the details described in the previous steps.
very high number of studies, it was then needed return to
an ascending method allowing the results’ refinement and Results
to maintain the update.
The exclusion of articles was mainly based on the rele- Five main categories could be identified through the lit-
vance to the subject regarding to the research question, thus erature analysis: physiological and pathological, neuropsycho-
reducing the interpretation biases and deficient protocols. logical, lifestyle, non-modifiable and environmental factors.
The second selection criterion followed the proof level pyra- Beneficial and deleterious effects of high and low HRV were
mid according to the scientific validity of each study, men- presented, respectively, when possible. Each category was de-
tioned above. Over 150 reviews and articles were analyzed, tailed accordingly with significant conclusions in order to de-
87 were finally selected and 56 are presented within this ar- termine the cause-to-effect relationship between each factor
ticle. Any article that could not explicitly reveal the needed and HRV and if these links could be considered as significantly
scientific validity criteria, such as abstracts or conference pa- harmful or beneficial, or as not significant enough to draw a
pers, was excluded. conclusive remark. In such cases, recommendations were
made, respectively.
Influence diagram
Heart rate variability and neurological pathways
An influence diagram aims to graphically represent the
statistically significant cause-to-effect links between the dif- Cardiac innervation
ferent elements as well as with the harmful effects. There
are several techniques, based on causes, consequences or Briefly, the heart intrinsic neural network is composed of
events, allowing linking of the causes to the consequences. many subpopulations of specialized cells (nodes) able to gen-
The method chosen for this literature overview was based on erate electric currents spontaneously while the extrinsic of
the root cause analysis tree creation in order to identify the cardiac innervation regroup the efferences and afferences of
direct actors influencing HRV (4). This approach is simple to the autonomic nervous system (ANS) with the sympathetic
use, favors the systematic aspect of research of causes and (SANS) and parasympathetic (PANS) (mainly the vagus nerve
their links, and does not need chronological relationships be- [X]) divisions (5).
tween the factors and their effects.
The creation of the influence diagram was carried out us- Central control of HRV
ing an iterative process in 4 steps (Fig. 1).
Besides X’s nuclei, several endocranial structures play a
- Step 1: Literature review and analysis. preponderant part in HRV modulation. In different literature
- Step 2: Categorization. Two levels of classification were reviews and MRI studies, Thayer et al (6-9), could identify the
used: main ANS actors linked with HRV.
• First, all elements could be undertaken whether the Moreover, Thayer et al (6, 7, 10), through reviews and
factor was associated with an intrinsic parameter meta-analyses over 10 neuroimaging datasets, confirmed the

© 2016 The Authors. Published by Wichtig Publishing

e34 Influence diagram of factors related to heart rate variability

Fig. 2 - Schematization of the affer-

ences and efferences between some
ANS actors and HRV. Round dotted
arrows indicate afferences, plain
arrows indicate efferences while
squared dotted arrows indicate both
ways communication between the
related structures. Low frequency
(LF) band (red arrows) corresponds
to the sympathetic share of the HVR
specter, while the high frequency
(HF) band (green arrows) is asso-
ciated with the parasympathetic
share, distributed through the vagus
nerve mainly. Very low frequency
(VLF) band (blue arrows) is still un-
der consideration but can be related
to the cardiac autonomous nervous
system (ANS).

regions consistently associated with HRV and even proposed community, thus allowing comparisons of datasets. In fact,
a neurovisceral integration model to better understand the different analytic parameters can be extracted, such as the
neuronal activation and inhibition effects of ANS actors on standard deviation normal to normal or root mean square of
the heart. On another side, the recent review proposed by successive differences. The latter was actually recognized to
McCraty and Childre (11) also resulted in the presentation of accurately estimate the changes in HRV due to nervous infor-
the known afferences from the heart and vascular system to- mation carried out by the vagal nerve (12).
wards the CNS.
By combining the heart anatomy (5) with the structures Frequency analysis
identified by Thayer et al and by McCraty et al, Figure 2 was
built to briefly schematize the main actors involved in HRV The representation of HRV basically comes from the re-
modulation, including the hypothalamus, nucleus tractus sol- port of RR intervals from electrocardiograms (ECGs) versus
itarii (NTS, nucleus of the solitary tract), periaqueductal gray time. Many studies (13, 14) showed that HRV can be analyzed
matter, amygdala, thalamus, dorsal vagal complex, prefrontal, under two major frequency bands: high frequencies (HF)
insular and cingulate anterior cortices. (0.15-0.4 Hz) and low frequencies (LF) (0.04-0.15 Hz), associ-
Such schematic representation already suggests the com- ated with ANS. While LF was found to be a poor marker of
plexity of heart-brain connections but can help clinicians to sympathetic tone but was rather related to baroreflex activ-
identify neurological disorders resulting in HRV decreases. ity (15), HF seems to consistently correspond to parasympa-
Moreover, even if many structures were identified, the un- thetic tone (12, 16, 17). HRV can be used as a health index, a
derlying mechanisms linking the heart to the brain (and recip- biofeedback tool and a mean to report on the ANS-CNS inte-
rocally) are more complex and yet to be fully elucidated (9). gration (8).
Over recent years, and with Dr J. Andrew Armour research,
Heart rate variability analysis a new theory suggests that the network regrouping all the car-
diac neurons, neuronal connections, and the neurotransmit-
Temporal analysis ters, actually constitutes a brain as such. This complex circuit
is able to manipulate information independently of central
The other and the simplest way to analyze HRV data is in and autonomous controls, and was correlated with the very
the carry out time domain method. Even if it does not provide low frequency part of the spectrum (0.0033-0.04 Hz) (18-21).
any quantifiable insight in the autonomous tone and balance, Another band, the ultra-low frequency band (below
it is still widely used and recognized among the scientific 0.0033 Hz), can only be extrapolated with 24-hour recordings

© 2016 The Authors. Published by Wichtig Publishing

Fatisson et al e35

(22). Yet their physiological components need to be fully de- who seem to be more sympathetically responsive (31), the
termined. Consequently, based on this limited information, mechanisms underlying the relationship between HRV and
future investigations are needed, while the major bands might sexual hormones are yet to be completely elucidated.
be more useful tools for daily clinical assessment of HRV. Moreover, a preliminary study (32) reported a decrease
in salivary cortisol for subjects practicing self-emotional man-
Cardiac coherence agement program, correlated with in an increase in coherent
state in HRV signals.
While physiological HRV is represented by an irregular fre- Based on the analyzed studies, it would seem that the re-
quency versus time curve (named as chaotic), a specific state lationships of the thyroid, sexual hormones or cortisol with
(often due to a regular or controlled respiration) induced the HRV are established and significant in some cases, therefore
heart rate to describe a sinusoidal curve around 0.1 Hz. This useful for such investigation, but their nature seems rather
state is referred as coherence or resonance. The spectral complex and needs to be clarified with future extended and
analysis of such state gives a high peak in the LF band and specific review.
none in the HF or VLF bands. According to McCraty and col-
leagues at the Heart Math Institute (HMI), heart coherence Respiratory factors
is a manifestation of physiological coherence (a term intro-
duced by these researchers) and allows the improvement of Another factor greatly influencing HRV is due to tho-
individual self-regulatory processes (12). racic respiration (33). A physiological phenomenon happens
The primary objective of this review is to list the factors at each respiration: the respiratory sinus arrhythmia (RSA)
directly linked to HRV. The analysis of the effects of cardiac where heartbeat increases as the air is breathed in and de-
coherence (CC), in addition to increase physiological ampli- creases at each expiration.
tude of HRV and reduce stress, was already carried out in In 1999, van Ravenswaaij-Arts et al (33) proposed a sim-
detail by the HMI researchers. One of their reviews on the ple schematization of the heart-brain interactions, involving
subject was published in 2015 and describes with precision many actors participating in RSA, such as baroreflexes, blood
the benefits of CC (23). Therefore, when applicable, only pressure (BP) and chemoreceptors. More recently, a literature
specific effects of CC are mentioned accordingly throughout review detailed two main mechanisms to describe RSA (34),
this article. involving tonic and phasic chemo- and, barometric reflexes,
heart and lung stretching reflexes, some local metabolic
Physiological and pathological factors ­factors, central generators of heart rhythm and the corre-
sponding nerves (X particularly) (35). Such studies underlined
Recently, it was analyzed, reviewed and concluded that different structures involved in heart-brain interactions and
a low HRV, through deficient cholinergic reflexes or through influencing HRV. It is however important to mention that RSA
pro-inflammatory cytokines, in the long term leads to im- is also influenced by several factors (age, gender, ethnicity,
mune dysfunction and inflammation in addition to CVD or posture, cardio-pulmonary function), these same variables
depression (1, 8). Besides the nervous actors and these re- can also in turn affect HRV (34).
flexes, other physiological elements and their pathological Based on these models (33, 34), it is logical to stipulate
correspondents can influence the HRV: endocrine, respira- that respiratory pathologies may in turn affect HRV. In fact,
tory, cardiovascular and neurological factors. and for example, asthma has been linked to reduced HRV in
children (36).
Endocrine factors
Neurological factors
By considering the reciprocal messages between the
heart and the rest of the body, the hormones are amongst As presented previously, neural connections between the
the messengers worth mentioning and briefly detailed. heart and the brain are numerous. If one of these structures
Although their potential benefits to patients affected by is affected, it is logical to expect that HRV will be as well. In
CVDs (24), a recent controlled study reported that thyroxin fact, neurological disorders, associated with brain damage,
treatments for epithelial cancers can decrease HRV signifi- were linked with an HRV decrease: Parkinsonian syndrome,
cantly (25), actually confirming recent results on hypothy- spinocerebellar degeneration, Shy-Drager syndrome, mul-
roidism (26). In fact, thyroid hormones have direct effects on tiple sclerosis, Guillain-Barré syndrome (33).
the myocardium by increasing its contractility but also on the In turn, not only cardiac coherence (CC) biofeedback
ANS by altering the sympathetic response (27). could equilibrate ANS, favor immune function, but also could
On another side, estrogen levels were significantly correlat- improve academic performances and other cognitive func-
ed with HRV measures in healthy women, thus confirming the tions such as memory (11, 23). A recent transversal study
cardioprotective effect of feminine sexual hormones (28). Ad- suggested that CC could possibly facilitate neurocortical reor-
ditionally, masculine androgens have a beneficial effect (para- ganization, even if would be difficult to confirm (37).
sympathetic) on the heart autonomous modulation (higher Consequently, based on all these results, one could
HRV with high testosterone levels) (29) while estradiol tends to possibly hypothesize that increasing HRV could potentially
preferably induce a parasympathetic activity (30). Consequent- have a ­beneficial effect on the symptoms, on the rate of
ly, even if a literature analysis confirmed that women tend to the neurological disease, or at least on the risk factors to
have a greater parasympathetic response capacity than men, develop such disorders.

© 2016 The Authors. Published by Wichtig Publishing

e36 Influence diagram of factors related to heart rate variability

Cardiovascular diseases (CVD) Consequently, based on these observations, it is safe to

assume, given the other known benefits of exercise therapy,
To be able to detect CVD is as important as understanding that this factor can improve HRV in populations varying from
their etiology. For many years, several research teams have CVD patients to athletes.
used HRV as an indicator of these types of pathologies.
In their systematic review, Thayer et al (38) studied in de- Alcohol, tobacco and drug consumption
tail the risk factors of CVD and noted that epidemiological
studies tend to confirm that HRV is lower for subjects with Alcohol and tobacco consumption also have an effect on
high BP rather than for subjects with normal BP. A similar re- HRV. Chronic smokers and alcohol drinkers have a low HRV
lationship could be established with a high level of blood cho- but this effect is reversible when they stop drinking alcohol
lesterol or glucose (diabetes) and a decreased HRV. or smoking (38, 39).
This review coupled with other studies and reviews con- Regarding alcohol, it induces an HRV decrease, which
firmed that a decreased HRV is an indicator of CVD (1, 14, could be related to a sympathetic activation or a parasympa-
38-40). Therefore, it was not relevant to detail further the thetic inhibition (14). This observation was confirmed in over
now recognized relationship between CVD and low HRV. 542 healthy subjects separated into two groups according to
their alcohol consumption level (high or low) (46). In fact, this
Other factors study revealed that high alcohol consumption is associated
not only with a decreased HRV, but also with a high cortisol
The model proposed by van Ravenswaaij-Arts et al (33) level, suggesting the possible implication of the hypothala-
involves the renin-angiotensin system and also the thermo- mo-hypophyseal-adrenal axis in this phenomenon.
regulation. A literature review of HRV identified many param- There are several studies on the use of different medica-
eters influencing HRV, such as body temperature. In fact, if tion and drugs and some examples can show how drugs can
the temperature decreases enough, it induces a bradycardia influence HRV. In particular, a quantitative review on antide-
(this phenomenon is actually applied for open-heart surgery) pressants revealed that tricyclic medication significantly de-
(41). Alternatively, when temperatures rise, such as with fe- creased HRV in studies on which recording was carried out
ver, heart beats accelerate. Consequently, this aspect points on short time intervals (47). Depending on medication type
out that the ANS and CNS are not the only regulators of HRV and population, results can greatly vary. Besides, a quantita-
- other physiological factors are also involved. tive review concluded that the necessary sample to obtain
significant HRV changes could need 660 patients taking con-
Lifestyle factors ventional medication to treat coronary dysfunctions (beta-
blockers, calcium channel blockers, angiotensin-converting
Physical activity enzyme inhibitors) (48). Necessarily, the cause-to-effect link
between medication and HRV was established but its nature
Interestingly, significant results, analyzed by several litera- would need to be clarified with large-scale populations and
ture reviews, were obtained to validate the increase of heart- with different category of medication. Since the reverse ben-
beat from lying down position to seated position and from eficial effect of CC on tobacco users was studied, it would
seated to standing up positions (14, 33, 39). also be interesting to replicate the experiments with heavily
Physical activity, which action can vary from one indi- medicated subjects.
vidual to another, is known to change HRV (39) by decreas-
ing sympathetic activation (40). The Whitehall study (42) Meditation
noted that HRV was found to be higher (and cardiac rhythm
lower) in subjects having physical activity from moderate- Recent studies reported that HRV could be used as an
to-vigorous. indicator of meditative state (37). Moreover, in a transversal
Moreover, a quantitative link was established between the study in over 14 subjects in 2014, they reported that auto-
ultra-low frequency band and muscle activity (43). ­Voluntary genic meditation (also called “Schultz’s autogenic training”)
restriction of physical activity resulted in a decrease of this leads to an increase of CC score (ratio of medium frequencies
band power, thus suggesting the need to include physical ac- over the sum of LF and HF), and of alpha, beta and gamma
tivity in future ambulatory HRV studies. As such, a recent re- brainwaves. According to these results, it indicates a stron-
view suggested that supervised and non-supervised exercise ger structural or functional connection between cortical and
therapy could increase HRV in patients affected by CVDs and thalamic regions, as previously presented (Fig. 2). In a trans-
diabetes mellitus (44). The authors pointed out the possible versal study (49), the coherence ratio (HF/LF) significantly in-
implication of angiotensin and Nitric Oxide (NO) in the physi- creased after a meditation practice by Vipassana experts. This
ological mechanisms as well as the need for further under- increase was also correlated with a greater attention commit-
standing of such mechanisms. ment and a reinforced autonomous regulation (ANS).
On the opposite side, even if the short-term and long-
term effects of training in athletes remain to be clarified, this Non-modifiable factors
population can show various HRV profiles, thus confirming
the usefulness of HRV as a tool to monitor their physiology. With age, HRV decreases. This is a known fact confirmed
However, much care in methodology is needed when design- by a quite recent systematic literature review (38). Even if
ing analyzing studies with athletes (45). the underlying mechanism is yet to be elucidated, some

© 2016 The Authors. Published by Wichtig Publishing

Fatisson et al e37

researchers think that it might be related to ANS maturation needs to be mentioned that the evaluation of stress should
and that this decrease seems to affect women more than be standardized, which is still not the case, since stress is mul-
men (14). tifactorial (10).
No specific study was specifically dedicated to the influ- With a systematic approach, it was possible to list many
ence of ethnicity on HRV. However, the systematic review of stress sources inducing low HRV, such as anxiety, hostility,
Thayer et al (38) mentioned that the studies they analyzed depression, but an emerging source recently gained atten-
were normalized with age, gender and ethnicity. Indirectly, tion - work stress. In fact, many analyzed studies revealed a
this indicates that ethnicity (or more generally genetics) has significant correlation between a high level of work stress
an influence on BP and consequently on HRV. This aspect is and low HRV. This remains the case even by using several
now well known by the scientific community without need to variables (gender, alcohol consumption, education level,
be a detailed object of this literature overview. work characteristics, etc.). Besides, the same stress was
To the authors’ knowledge, the literature observing the also correlated with a higher risk of CVD and a high cardiac
effect of genetics on HRV is relatively limited. Nevertheless, rhythm (38).
two studies were conducted to examine the heritability of
HRV and the results highlighted the contribution of genetics Depression
within the ANS activity (50, 51). Another study pointed out
that ethnic differences have an effect on HRV during youth, From a recent meta-analysis, Kemp et al (55) obtained a
while no differences were observed for gender (52). Con- significant correlation (p<0.001) between depression and a
sequently, whilst heritability seems to be a factor to be ac- low HRV. They also verified the effects of many antidepres-
counted for when analyzing very specific traits on HRV, this sants and the result was identical for tricyclic medication.
relationship needs further clarification and future research. They also emphasized for the need for long-term studies.
The low HRV value, even if depression is not associated
Environmental factors with a CVD, remains an indicator of poor health (23, 55). How-
ever, the affect is reversible in this case. In fact, in a controlled
A recent systematic review actually established a detailed transversal study on 24 subjects, a significant (p<0.05) return
list of work-related factors that can influence HRV (53). Among to a higher HRV was observed when depressed patients used
these factors there is particulate matter, several chemical a biofeedback approach.
components, electromagnetic fields (EMF), vibrating tools,
psychosocial charge, working time, fatigue, etc. A prolonged Negative emotions
exposure to these factors leads to a decrease in HRV.
Further literature analyses would need to examine the ef- In psychology, neuroticism is associated with the experi-
fect of these factors on the specific physiological structures ence of negative emotions and concerns patients suffering
identified by Thayer and coworkers and others, but also on from anger, depression or anxiety (56). A transversal study on
the other categories presented here, in order to understand 33 healthy subjects confirmed the significant correspondence
the underlying mechanisms of such effect. between weak neuroticism (negative emotions) and low HRV
Considering that modern lifestyles involve the use of and the inverse as well (57).
many electronic devices and wireless connections and that While negative emotions, such as anger, anxiety, frustra-
HMI researchers pointed out the interaction between elec- tion and worry produce every irregular ECG and a reduced
tromagnetic human heart fields (11), the daily exposure to HRV, it is also worth mentioning the benefits obtained by
EMF generated by electronic devices and their effect on hu- negative emotions by practicing CC (23). Even if the underly-
man physiology should also be the subject of future research. ing mechanism remains unknown, the reversibility of cardio-
vascular after-effects (due to negative emotions) by positive
Neuropsychological factors emotions was first demonstrated in 2000 and then confirmed
in 2010 by Fredrickson and Levenson (58). Kemp and Quin-
Another group of endocranial structures was identified tana (1) also concluded that HRV holds a significant functional
and behavior (social, intentional, affective, executive) by importance on social behavior, self-regulation and psycholog-
modulating motivation from external and internal stimuli ical flexibility against life stressors.
(54). Among this network, there are the anterior cortex, the
amygdala, the insula, the periaqueductal grey matter, which Discussion
are also structures regulating HRV (as pointed out by Fig. 2).
Consequently, and from a general point of view, HRV is linked Themes identified
to personality but a list of neuropsychological factors influ-
encing HRV is not limited to this aspect and actually includes Synthesis of literature review
stress, depression and negative emotions.
The data analyzed in this exhaustive literature review
Stress on physiological, environmental and psychological elements
linked with HRV are regrouped by category and presented in
With a brief research on stress, one can realize quickly Figure 3, with an influence diagram. The aim of this diagram
that numbers contradict each other, without further details. is to synthesize the information schematically in order for it to
However, stress can be the most dominant factor, and it be used for research protocols, eventually.

© 2016 The Authors. Published by Wichtig Publishing

e38 Influence diagram of factors related to heart rate variability

Fig. 3 - Influence diagram of

cause of effect factors linked
with heart-rate variability
(HRV). The direction of the
arrows indicates a cause-to-
effect link between related
factors. While red arrows
indicate a deleterious effect
and green or blue arrows a
beneficial one, purple arrows
refer to a link for which the
effect can be deleterious or
beneficial. Blue arrows are
specific to the heart coher-
ence state. Red, green and
blue arrows correspond to
significant effects while grey
arrows indicate a link for
which statistical significance
was not achieved.

This diagram emphasizes the importance of the brain- therefore natural that such parameter is the base of many
heart interaction from the additional connections and the meditative techniques designed to improve HRV by favor-
overlapping between physiological and neuropsychological ing coherent states.
factors. In fact, besides the multiple nervous links (Fig. 2), Besides, since literature underlines, many interac-
heart and brain also communicate through neurotransmit- tions exist between HRV and the central nervous system
ters, hormones but also through EMF. As observed and con- (CNS). Moreover, some neuropsychological factors can
firmed by (23), electromagnetic waves generated by the involve other CNS elements, which can influence the iden-
heart in coherent state are immediately recorded by brain tified elements of ANS. Experts in this domain, already ac-
waves. The subject of EMF is still poorly studied and needs knowledge that not all the mechanisms are well described
specific and expensive instruments. and understood and that much research is needed in or-
This heart-brain communication could also be involved der to clarify the implication of CNS and its links with the
in neurodegenerative diseases (NDD). In fact, even if the heart.
mechanisms remain uncertain, the analyzed research Most selected texts are reviews and meta-analyses rela-
proves that there is a vascular etiology between Alzheimer’s tively specialized but very detailed in each domain. The origi-
disease (AD) and vascular and cardiac dysfunctions (59). The nality of this research is found in the synthesis and compilation
same author even questions the classification of AD under of all the scattered information and its potential usefulness for
the NDD category and suggests that AD be seen as a CVD daily clinical practice as well as for designing methodologically
(60). According to their literature review, one of the po- precise research protocols.
tential mechanisms would involve the incorrect folding of
­proteins. The authors even suggest the term “Alzheimer’s Other aspects reflecting the existing literature
cardiac disease” to name some CVD. These observations
bring us to think if brain degeneration is a cause or a conse- In fact, most of research conducted on HRV consists of
quence of NDD. crossed or transversal studies, valid but easier to carry out.
In both cases, statistical tests are necessary to obtain trust-
Complexity of the system and originality of the research ful results. In transversal studies, the tested populations are
only a sample of the general population at a given time, lead-
As presented by Figure 3, HRV surrounding system is ing to difficulties in generalizing and extending the results.
multifactorial. From the selected literature, some links al- For crossed studies, the lack of a control group brings issues
ready appear, such as between respiration and emotions for results comparison. This aspect underlines, as many re-
or posture, or mood or age. The fact is, respiration holds searchers suggested (53), a lack of longitudinal studies, in or-
a particular key role in the regulation of HRV. Since it is a der to know the long-term effects (harmful or beneficial) of
physiological parameter that anyone can control, it seems these factors on HRV.

© 2016 The Authors. Published by Wichtig Publishing

Fatisson et al e39

Critic on research 5. Laske TG, Shrivastav M, Iaizzo PA. The cardiac conduction sys-
tem. In: Iaizzo PA, ed. Handbook of cardiac anatomy, physiol-
As mentioned earlier, the originality of this study can be ogy and devices. Springer Science+Business Media. LLC 2009;
found in the gathering of scattered data from each respective 11:159-175.
6. Thayer JF, Lane RD. Claude Bernard and the heart-brain connec-
domain and to present the main factors directly influencing
tion: further elaboration of a model of neurovisceral integration.
HRV into a visual and easily usable representation. In front of Neurosci Biobehav Rev. 2009;33(2):81-88.
the magnitude of the work, it was not possible to exhaustively 7. Thayer JF, Lane RD. A model of neurovisceral integration in
determine the indirect links between the different categories. emotion regulation and dysregulation. J Affect Disord. 2000;
Consequently, future research in this area should focus on 61(3):201-216.
identifying the reinforcement links and to further detail the 8. Thayer JF, Brosschot JF. Psychosomatics and psychopathology:
influences between each category. Even if some factors need looking up and down from the brain. Psychoneuroendocrinol-
further investigation, the identified link could still be of use ogy. 2005;30(10):1050-1058.
for daily clinical assessment. 9. Lane RD, McRae K, Reiman EM, Chen K, Ahern GL, Thayer JF.
The limit accorded to this study in terms of the identi- Neural correlates of heart rate variability during emotion. Neu-
roimage. 2009;44(1):213-222.
fication of the direct links only, cannot consequently show
10. Thayer JF, Åhs F, Fredrikson M, Sollers JJ III, Wager TD. A meta-
the strengthening effects due to the multiple possibilities of analysis of heart rate variability and neuroimaging studies: im-
relationships between each different factor. However, this plications for heart rate variability as a marker of stress and
limitation also could eliminate any overflow towards ANS health. Neurosci Biobehav Rev. 2012;36(2):747-756.
since HRV could be used as an indicator of ANS balance. 11. McCraty R, Childre D. Coherence: bridging personal, social, and
Moreover, the mechanisms linking HRV and others factors global health. Altern Ther Health Med. 2010;16(4):10-24.
are still poorly understood and much is to understand if 12. McCraty R, Shaffer F. Heart Rate Variability: New Perspectives
the HRV changes are related to these different factors in a on Physiological Mechanisms, Assessment of Self-regulatory
causal or effective manner. Capacity, and Health risk. Glob Adv Health Med. 2015;4(1):
Internal validity can be obtained with a more detailed 46-61.
13. Ahmad S, Tejuja A, Newman KD, Zarychanski R, Seely AJ. Clini-
analysis of several studies in order to confirm the links estab-
cal review: a review and analysis of heart rate variability and
lished in Figure 3. External validity cannot be obtained since the diagnosis and prognosis of infection. Crit Care. 2009;13(6):
too many inter- and intra-category links remain uncertain. A 232-238.
meta-analysis could be adequate to confirm the reliability of 14. Rajendra Acharya U, Paul Joseph K, Kannathal N, Lim CM,
such diagram in front the unique and multifactorial complex- Suri JS. Heart rate variability: a review. Med Biol Eng Comput.
ity of such a system. 2006;44(12):1031-1051.
15. Goldstein DS, Bentho O, Park M-Y, Sharabi Y. Low-frequency
Conclusion and future perspectives power of heart rate variability is not a measure of cardiac
sympathetic tone but may be a measure of modulation of car-
As summarized by this study, the group of factors influ- diac autonomic outflows by baroreflexes. Exp Physiol. 2011;
96(12):1255-1261.
encing HRV is multifactorial and could give a preliminarily
16. Napadow V, Dhond R, Conti G, Makris N, Brown EN, Barbieri R.
exhaustive portrait of this system thanks to the influence of Brain correlates of autonomic modulation: combining heart rate
diagram creation The main categories standing out from this variability with fMRI. Neuroimage. 2008;42(1):169-177.
study (physiological/pathological, neuropsychological, non- 17. Åhs F, Sollers JJ III, Furmark T, Fredrikson M, Thayer JF. High-­
modifiable, lifestyle and environmental factors) are interde- frequency heart rate variability and cortico-striatal activity in
pendent, hence the complexity of the system. Such interde- men and women with social phobia. Neuroimage. 2009;47(3):
pendency definitely needs to be further detailed. 815-820.
18. Rosen MR, Cohen IS, Danilo P Jr, Steinberg SF. The heart re-
Disclosures members. Cardiovasc Res. 1998;40(3):469-482.
19. Huang M-H, Friend DS, Sunday ME, et al. An intrinsic adren-
Financial support: The authors would like to thank the Fondation ergic system in mammalian heart. J Clin Invest. 1996;98(6):
canadienne pour l’enseignement et la recherche en ostéopathie for 1298-1303.
participating in the publishing fees. 20. Armour JA. Neurocardiology - Anatomical and functional prin-
Conflict of interest: The authors declare no conflict of interest. ciples, 2003, HeartMath Research Center, Institute of Heart-
Math: Boulder Creek, CA. Publication No. 03-011.
References 21. Armour JA, Kember GC. Cardiac sensory neurons. In: Armour
JA, Ardell JL, eds. Basic and clinical neurocardiology. New York:
1. Kemp AH, Quintana DS. The relationship between mental and Oxford University Press. 2003:79-117.
physical health: insights from the study of heart rate variability. 22. Kleiger RE, Stein PK, Bigger JT Jr. Heart rate variability: mea-
Int J Psychophysiol. 2013;89(3):288-296. surement and clinical utility. Ann Noninvasive Electrocardiol.
2. Randolph JJ. A Guide to writing the dissertation literature review. 2005;10(1):88-101.
Practical assessment, research and evaluation 2009;14(13):1-13. 23. McCraty R, Atkinson M, Tomasino D, Bradley RT. The coherent
3. Boote DN, Beile P. Scholars before researchers: on the central- heart heart–brain interactions, psychophysiological coherence,
ity of the dissertation literature review in research preparation. and the emergence of system-wide order. Integral Review.
Educational Researcher. 2005;34(6):3-15. 2009;5(2):10-115.
4. Wilson PF, Dell LD, Anderson GF. Root cause analysis: a tool for 24. Fazio S, Palmieri EA, Lombardi G, Biondi B. Effects of thyroid
total quality management. Milwaukee, Wisconsin: ASQ Quality hormone on the cardiovascular system. Recent Prog Horm Res.
Press; 1993. 2004;59(1):31-50.

© 2016 The Authors. Published by Wichtig Publishing

e40 Influence diagram of factors related to heart rate variability

25. Shuvy M, Arbelle JE, Grosbard A, Katz A. A simple test of 43. Serrador JM, Finlayson HC, Hughson RL. Physical activity is a
one minute heart rate variability during deep breathing for major contributor to the ultra low frequency components of
evaluation of sympatovagal imbalance in hyperthyroidism. Isr heart rate variability. Heart. 1999;82(6)(e9):e9.
Med Assoc J. 2008;10(8-9):603-606. 44. Routledge FS, Campbell TS, McFetridge-Durdle JA, Bacon SL.
26. Celik A, Aytan P, Dursun H, et al. Heart rate variability and heart Improvements in heart rate variability with exercise therapy.
rate turbulence in hypothyroidism before and after treatment. Can J Cardiol. 2010;26(6):303-312.
Ann Noninvasive Electrocardiol. 2011;16(4):344-350. 45. Aubert AE, Seps B, Beckers F. Heart rate variability in athletes.
27. Polikar R, Burger AG, Scherrer U, Nicod P. The thyroid and the Sports Med. 2003;33(12):889-919.
heart. Circulation. 1993;87(5):1435-1441. 46. Thayer JF, Hall M, Sollers JJ III, Fischer JE. Alcohol use, urinary
28. Leicht AS, Hirning DA, Allen GD. Heart rate variability and en- cortisol, and heart rate variability in apparently healthy men:
dogenous sex hormones during the menstrual cycle in young Evidence for impaired inhibitory control of the HPA axis in
women. Exp Physiol. 2003;88(3):441-446. heavy drinkers. Int J Psychophysiol. 2006;59(3):244-250.
29. Wranicz JK, Rosiak M, Cygankiewicz I, Kula P, Kula K, Zareba W. 47. van Zyl LT, Hasegawa T, Nagata K. The effects of antidepressants
Sex steroids and heart rate variability in patients after myocardial on heart rate variability in major depression: a quantitative re-
infarction. Ann Noninvasive Electrocardiol. 2004;9(2):156-161. view. Biopsychosoc Med. 2008;30(2):12-22.
30. Doğru MT, Başar MM, Yuvanç E, Simşek V, Sahin O. The rela- 48. Nolan RP, Jong P, Barry-Bianchi SM, Tanaka TH, Floras JS. Ef-
tionship between serum sex steroid levels and heart rate vari- fects of drug, biobehavioral and exercise therapies on heart
ability parameters in males and the effect of age. Turk Kardiyol rate variability in coronary artery disease: a systematic review.
Dern Ars. 2010;38(7):459-465. Eur J Cardiovasc Prev Rehabil. 2008;15(4):386-396.
31. Dart AM, Du X-J, Kingwell BA. Gender, sex hormones and au- 49. Delgado-Pastor LC, Perakakis P, Subramanya P, Telles S, Vila J.
tonomic nervous control of the cardiovascular system. Cardio- Mindfulness (Vipassana) meditation: effects on P3b event-relat-
vasc Res. 2002;53(3):678-687. ed potential and heart rate variability. Int J Psychophysiol. 2013;
32. McCraty R, Barrios-Choplin B, Rozman D, Atkinson M, ­ 90(2):207-214.
Watkins AD. The impact of a new emotional self-management 50. Singh JP, Larson MG, O’Donnell CJ, Tsuji H, Evans JC, Levy D.
program on stress, emotions, heart rate variability, DHEA and Heritability of heart rate variability: the Framingham Heart
cortisol. Integr Physiol Behav Sci. 1998;33(2):151-170. Study. Circulation. 1999;99(17):2251-2254.
33. van Ravenswaaij-Arts CM, Kollée LA, Hopman JC, Stoelinga GB, 51. Kupper NHM, Willemsen G, van den Berg M, et al. Heritabil-
van Geijn HP; Ravenswaaij-Arts CMAv. Heart rate variability. ity of ambulatory heart rate variability. Circulation. 2004;110
Ann Intern Med. 1993;118(6):436-447. (18):2792-2796.
34. Yasuma F, Hayano J. Respiratory sinus arrhythmia: why does the 52. Wang X, Thayer JF, Treiber F, Snieder H. Ethnic differences and
heartbeat synchronize with respiratory rhythm? Chest. 2004; heritability of heart rate variability in African- and European
125(2):683-690. American youth. Am J Cardiol. 2005;96(8):1166-1172.
35. Berntson GG, Cacioppo JT, Quigley KS. Respiratory sinus arrhyth- 53. Togo F, Takahashi M. Heart rate variability in occupational health
mia: autonomic origins, physiological mechanisms, and psy- —a systematic review. Ind Health. 2009;47(6):589-602.
chophysiological implications. Psychophysiology. 1993;30(2): 54. Devinsky O, Morrell MJ, Vogt BA. Contributions of anterior cin-
183-196. gulate cortex to behaviour. Brain. 1995;118(Pt 1):279-306.
36. Kazuma N, Otsuka K, Matsuoka I, Murata M. Heart rate vari- 55. Kemp AH, Quintana DS, Gray MA, Felmingham KL, Brown K,
ability during 24 hours in asthmatic children. Chronobiol Int. Gatt JM. Impact of depression and antidepressant treatment
1997;14(6):597-606. on heart rate variability: a review and meta-analysis. Biol Psy-
37. Kim D-K, Rhee J-H, Kang SW. Reorganization of the brain and chiatry. 2010;67(11):1067-1074.
heart rhythm during autogenic meditation. Front Integr Nuero- 56. Jeronimus BF, Riese H, Sanderman R, Ormel J. Mutual rein-
sci. 2014;7:109. forcement between neuroticism and life experiences: a five-
38. Thayer JF, Yamamoto SS, Brosschot JF. The relationship of au- wave, 16-year study to test reciprocal causation. J Pers Soc
tonomic imbalance, heart rate variability and cardiovascular Psychol. 2014;107(4):751-64.
disease risk factors. Int J Cardiol. 2010;141(2):122-131. 57. Di Simplicio M, Costoloni G, Western D, Hanson B, Taggart P,
39. Valentini M, Parati G. Variables influencing heart rate. Prog Harmer CJ. Decreased heart rate variability during emotion
Cardiovasc Dis. 2009;52(1):11-19. regulation in subjects at risk for psychopathology. Psychol Med.
40. Lanfranchi PA, Somers VK. Arterial baroreflex function and 2012;42(8):1775-1783.
cardiovascular variability: interactions and implications. Am 58. Fredrickson BL, Levenson RW. Positive Emotions Speed Recov-
J Physiol Regul Integr Comp Physiol. 2002;283(4):R815-R826. ery from the Cardiovascular Sequelae of Negative Emotions.
41. Stauss HM. Heart rate variability. Am J Physiol Regul Integr Cogn Emotion. 1998;12(2):191-220.
Comp Physiol. 2003;285(5):R927-R931. 59. de la Torre JC; Torre JCdl. Alzheimer disease as a vascular disor-
42. Rennie KL, Hemingway H, Kumari M, Brunner E, Malik M, der: nosological evidence. Stroke. 2002;33(4):1152-1162.
Marmot M. Effects of moderate and vigorous physical activity 60. de la Torre JC; Torre JCdl. Is Alzheimer’s disease a neurodegen-
on heart rate variability in a British study of civil servants. Am J erative or a vascular disorder? Data, dogma, and dialectics.
Epidemiol. 2003;158(2):135-143. Lancet Neurol. 2004;3(3):184-190.

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