Space Weather Effects on Heart Rate Variations: Sex Dependence

Abstract

The effects of solar activity and the accompanying space weather events on human pathological conditions, physiological parameters and other psycho-physiological disturbances have been analyzed in numerous recent investigations. Moreover, many of these studies have particularly focused on the different physical reactions humans have, according to their sex, during variations in the physical environment. In the framework of the above, this work analyses heart rate data obtained from volunteers (687 men and 534 women) from three different regions (Athens, Piraeus and Heraklion) of Greece in relation to the geophysical activity and variations of environmental factors. Dst index and Ap index data, along with cosmic ray intensity data derived from the Athens Neutron Monitor Station (A.Ne.Mo.S.), were used. The study expands from April 2011 to January 2018, covering solar cycle 24. The ANalysis Of Variance (ANOVA) and the superimposed epochs methods were used in order to examine heart rate variations depending on sex. Results revealed that women tend to be more sensitive to physical environmental changes. Statistically significant results are related to the geomagnetic activity but were not obtained for cosmic ray variations.

1. Introduction

A few decades ago, Russian biophysicist Dr. A.L. Chizhevsky established the field of heliobiology to discuss the effects of the Sun’s activity on the human physiological state [1,2,3,4].

Since then, some of the main subjects of heliobiological studies have occasionally been:

(i)

Cardiovascular diseases [5,6,7,8,9,10];

(ii)

Ischemic strokes [11,12,13];

(iii)

Diseases of the nervous and other functional systems [14];

(iv)

Increased morbidity/mortality [15,16,17];

(v)

Human brain activity [18,19,20,21];

(vi)

Variations of human physiological parameters [22,23]; and finally,

(vii)

Psychology, concentration, reaction time, decision-making, and traffic accidents [24].

Moreover, many of these heliobiological investigations studied the response of the human organism to geophysical variations considering the factor of sex. For instance, how male and female organisms react during geophysical phenomena (geomagnetic storms and cosmic ray intensity variations). For example, some of the questions under discussion may explore if the impact of the effect is the same for both sexes if there is a time-dependent reaction in either of them, etc. [16,17,25,26,27,28,29].

For example, in [30], 16,683 men and women suffering from acute myocardial infarction were assessed in relation to solar activity indices (sunspot number and solar flux at 2.800 MGH and 10.7 cm wavelength), geomagnetic activity (GMA) parameters (Ap, Cp, Am), and cosmic ray activity. The results showed that there is a significant correlation between the number of acute myocardial infarctions per month and the three manifestations of heliogeophysical activity. More precisely, an inverse correlation was recorded for solar and GMA, and a positive correlation was recorded for cosmic ray activity. Concerning biological sex, the results for women were more significant and presented 2–3 times higher correlation coefficients than those for men.

As recorded in [31], the impact of space weather phenomena on the residents of the Russian settlements of the Barentsburg in the area of the Spitsbergen archipelago, which is located near the cusp region, was examined from 1985 until 1993. Among other results, it was concluded that female organisms showed high sensitivity to space weather variations in that region. High geomagnetic activity in the polar cusp was related to an increased number of pregnancy complications, etc.

In another study that was conducted by [28], the number of deaths due to suicide in the region of Northern Ireland from 1985 until 2010 was analyzed in relation to solar, interplanetary and geomagnetic activity parameters (i.e., sunspot numbers, solar flare index, sudden storm commencements, Ap and Kp indices). As a general result, the yearly mean of the heliogeophysical parameters mentioned above was well correlated to the number of deaths due to suicide of both men and women. However, for some of the parameters, men showed a large negative correlation, whereas women showed a good medium-negative correlation.

Furthermore, a large number of investigations have focused on one specific physiological parameter, i.e., arterial blood pressure. The different reactions of men and women to high GMA and cosmic ray intensity (CRI) variations were evaluated according to arterial systolic and diastolic blood pressure variations. For example, in a study by [32], 51 normotensive, healthy men and women in Mexico City, Mexico, were assessed during three geomagnetic storms, which developed in April and May 2008. The ANOVA and the superposed epoch analysis methods were applied to show that blood pressure response to GMA is statistically significant. Results revealed that the larger arterial blood pressure variations during geomagnetic storms referred to women and not men and were noticed two days before and one day after the storm (mainly for the systolic blood pressure).

The arterial blood pressure of 304 healthy normotensive men and women was studied in relation to the horizontal geomagnetic field component H during solar cycle 24 (2008–2014) in Mexico City. The methods of correlations, bivariate and superposed epochs analysis were applied. It was shown that important systolic and diastolic blood pressure changes were observed in women [33].

In a study by [34], essential hypertension was studied during disturbed space weather conditions (active geomagnetic conditions and solar wind speed exceeding 600 km/s). In total, 13,475 cards from emergency ambulance calls in the city of Kaunas, Lithuania, were evaluated for the time period 2009–2010. A multivariate Poisson regression method was applied. It was shown that during the aforementioned conditions, the registered number of emergency ambulance calls for elevated arterial blood pressure increased. This affected women and older patients the most.

Moreover, in [35], data on arterial systolic and diastolic blood pressure, heart rate, pulse pressure, and psycho-physiological complaints of 86 healthy men and women were examined during autumn 2001 and spring 2002. During these periods, high GMA was recorded. High GMA was connected to increased values of arterial blood pressure, pulse pressure and subjective psycho-physiological complaints. Subjective psycho-physiological complaints were more pronounced for women, proving that there is a higher sensitivity of women rather than men during strong GMA.

On the other hand, several studies conclude that either men are more responsive to heliophysical variations or that sex is not a significant factor in heliobiological investigations. For example, in [36], the arterial blood pressure of 77 healthy volunteers was examined during perturbations of the Earth’s magnetic field. Even though the arterial blood pressure of the volunteers under examination increased in relation to GMA (i.e., magneto-sensitive persons), no dependence was noticed based on age or sex, only on mild cardiovascular pathology.

Furthermore, the investigation of heart rate variability of a group of healthy men in subarctic regions showed that increased GMA was related to heart rate variability decrease [37,38]. The authors of [39] claimed that men presented higher myocardial infraction rates during Forbush decreases and severe geomagnetic storms, and [40] stated that the number of incidents of unstable angina per month correlated stronger with the Ap indices for men.

Finally, the daily arterial blood pressure data of eight hypertensive men and women in regard to the daily horizontal geomagnetic field component H were studied in [41]. The analysis took place in Mexico City, Mexico, in 2014 when a geomagnetic storm occurred. It was reported that variations in the geomagnetic field affected men more than women, underlying a possible sex difference in blood pressure reaction to a geomagnetic storm.

Based on the aforementioned, it can be argued that heliobiological studies are complicated and can occasionally lead to conflicting results. This is because human health can be affected by a number of other factors apart from geophysical activity. However, this should not be seen as a drawback or a reason to reject these investigations.

The retrospective studies presented herein analyze a large amount of data (for example, frequency of deaths or acute myocardial infarction incidents) during a period of several years. On the other hand, direct measurements of physiological parameters (i.e., arterial blood pressure) on the individuals were evaluated for a certain time period (mostly disturbed periods). In all of these studies, solar phenomena, interplanetary conditions, geomagnetic disturbances, and cosmic ray variations were assessed. Scientific methods (for example, correlation coefficients, ANOVA, multivariate Poisson regression, and the superposed epoch analysis) were used to analyze the geophysical data in terms of medical data. Therefore, these investigations and their findings must be considered as supplementary data and not contradictory. Proper analysis and comparison of the results concerning the effect of geospace on human physiology from different geographical regions and different time periods will ensure accurate and reliable conclusions.

With this study, another cardiovascular physiological parameter, i.e., heart rate, is being assessed for different levels of geophysical activity depending on sex. It should be noted that the average adult heart rate varies from 70 to 85 bpm (beats per minute). However, this value depends on sex and is higher for women. Therefore, for an adult man and woman, the average heart rate is expected to be 70–72 bpm and 78–82 bpm, respectively.

In this work, heart rate data of men and women from Athens, Piraeus, and Heraklion, Greece, were analyzed in regard to variations of the geomagnetic field and the CRI. The analysis used geomagnetic data (Dst index and Ap index) and CRI data provided by the Athens Neutron Monitor Station (A.Ne.Mo.S.) of the National & Kapodistrian University of Athens (NKUA). The time period under investigation is from April 2011 to January 2018 (solar cycle 24). The two methods used in order to examine heart rate variations, depending on sex, are ANalysis Of Variance (ANOVA) and the superimposed epochs method.

2. Data and Method

2.1. Medical Data

Three hospitals across Greece participated in this analysis. The Hippocratio General Hospital in Athens, the cardiology clinics of Nikaia General Hospital in Piraeus and the Heraklion University Hospital in Crete provided the HR data. Moreover, information on the medical state of individuals who they treated was also provided. For the time period from April 2011 to January 2018 (i.e., solar cycle 24), 534 women with a mean HR of 72.5 ± 0.8 bpm and 687 men with a mean HR of 70.3 ± 0.6 bpm were examined. Daily HR data were obtained with a Holter electrocardiogram [42].

This database included information about the medical history, pathological state, and psycho-physiological conditions of the individuals. For example, data on medication, cardiovascular parameters such as atrial and ventricular systoles, complaints such as arrhythmias, headaches, etc., and other types of discomfort are essential information to be assessed while investigating space weather effects on human physiological states. It should be mentioned that individuals with a history of cardiovascular diseases or medical treatment concerning the cardiovascular system were initially excluded. Even though the human organism is not entirely controllable, in this way, some other factors that could affect the results were restricted.

2.2. Cosmic Ray Intensity Data

The Athens Neutron Monitor Station (A.Ne.Mo.S.) of the Faculty of Physics of the NKUA was implemented in 2000. It has been an established member of the European High-Resolution Neutron Monitor Database (NMDB; http://www.nmdb.eu, accessed on 29 April 2024) since 2011. A.Ne.Mo.S. (Super 6NM-64) stands out amongst the neutron monitors of the worlwide network because it was the fourth station to be able to provide real-time data on the internet, but also because of its special location (the only station in the Balkans and the eastern Mediterranean Sea). A.Ne.Mo.S. (altitude 260 m asl, and geographical coordinates 37°58′ N, 23°47′ E) is operated by the Athens Cosmic Ray Group and has proven its valuable contribution to the scientific research and educational procedure in recent decades.

A brief description of a neutron monitor’s operation is provided in the following. In neutron monitors, the special gas-filled proportional counters are surrounded by a moderator, a lead producer, and the reflector. The incident nucleonic component (protons and neutrons) of the secondary cosmic rays causes nuclear reactions in the lead, where ‘evaporation’ occurs and low-energy neutrons are produced. These neutrons with energies of the order of MeV are slowed down to thermal energies by the moderator, and in NM64-type counters, approximately 6% of these neutrons are finally recorded by the proportional counter tubes (http://www.nmdb.eu, accessed on 29 April 2024).

Pressure- and efficiency-corrected CRI data (counts/s) were obtained daily from the Athens Neutron Monitor Station. CRI was normalized according to the $CRI=\frac{{CRI}_{obs}-{CRI}_{aver}}{{CRI}_{aver}}$, where ${CRI}_{obs}$ is the observed CRI value and ${CRI}_{aver}$ is the mean value calculated for the time period under examination. CRI variations ranged from –6% decreases up to +3% increases. The analysis of HR data in relation to CRI variations includes (a) large Forbush decreases (magnitude greater than 4%), (b) small CRI decreases (magnitude less than 3%), (c) quiet periods of CRI, i.e., no registered events (0%) and (d) CRI increases.

In general, the energetic particles of cosmic rays can threaten human health since they can interact with cells and, as a result, damage molecules. In turn, damaged molecules may affect human tissue and organs. The health risks from cosmic rays may be short-term (high radiation doses mostly during human spaceflight outside the Earth’s magnetosphere) or long-term (low radiation doses which can potentially harm space missions and aircraft crews and passengers).

2.3. Geomagnetic Activity Data

Dst index (World Data Centre for Geomagnetism, Kyoto; https://wdc.kugi.kyoto-u.ac.jp/dstae/index.html, accessed on 29 April 2024) and Ap index (German Research Center for Geosciences, GFZ; https://www.gfz-potsdam.de/en/section/geomagnetism/data-products-services/geomagnetic-kp-index, accessed on 29 April 2024) values were processed.

According to the Dst- and Ap index daily values, the GMA was organized into five intensity levels, as described in

Table 1. Dst-and Ap index levels and the corresponding number of measurements.

Activity	Dst Levels	Dst Index Values (nT)	Number of Measurements (Women)	Number of Measurements (Men)	Ap Levels	Ap Index Values	Number of Measurements (Women)	Number of Measurements (Men)
Quiet	I0	Dst ≥ 0	94	118	I0	Ap < 8	273	366
Minor	I	−20 < Dst < 0	267	351	I	8 ≤ Ap < 15	125	168
Moderate	II	−50 < Dst ≤ −20	145	194	II	15 ≤ Ap < 30	101	118
Strong	III	−100 < Dst ≤ −50	27	23	III	30 ≤ Ap < 50	26	30
Severe	IV	Dst ≤ −100	1	1	IV	Ap ≥ 50	9	5

.

2.4. Statistical Method

To analyze the HR data, one-way analysis of variance (ANOVA) [43] and superimposed epochs or Chree analysis [44] were used. Generally, the ANOVA method tests for statistical significance between means by comparing variances. More precisely, the variation of the parameter X is not significantly affected by factor A. This means there is no statistically significant difference between the mean values of X at every A factor level. This is regarded as the null hypothesis. However, if such differences are detected, the null hypothesis is rejected.

While applying the one-way ANOVA method, the cardiovascular parameter HR was defined as the ‘dependent variable’, whereas Dst, Ap and CRI levels were defined as the ‘factors’ (i.e., independent variables). The effect of the geophysical activity levels on the physiological parameter was tested.

Before continuing with the description of the analysis, it should be noted that to apply the ANOVA method, a certain condition must be met, i.e., the dependent variable values (i.e., HR) should follow a normal distribution. To examine whether this stands for the samples under investigation, the Shapiro–Wilk test of normality (W_men = 0.983520, p_men = 0.000000 and W_women = 0.978731, p_women = 0.000000) was performed. As shown, both results confirm that there are no signs of non-normality in the samples, so the ANOVA method can be applied.

The null hypothesis considers that for every different level of geophysical activity (Dst level, Ap level and CRI level), the mean values of the dependent variable under study (HR) are the same, while the alternative hypothesis states that the geophysical activity levels affect the physiological parameter.

The statistical significance level will ultimately determine which of the two hypotheses is valid. The level of statistical significance is set at p < 0.05 by the software system used in this study. Therefore, the null hypothesis is accepted for a p-level greater than 0.05, whereas for a p-level less than 0.05, the null hypothesis is rejected. Consequently, the alternative hypothesis is accepted.

The calculated HR mean values for every factor level are presented in tables. The standard error in calculating the average value with a 95% confidence interval, the maximum and minimum HR values for this confidence interval, and the number of measurements in each factor level are also shown in these tables. These results are also presented graphically in Section 3.

The superimposed epoch method or the Chree analysis is a statistical analysis that evaluates the temporal distribution of a parameter (in this case, HR) during the development of an event (i.e., geomagnetic storm or Forbush decrease). ANOVA, along with the method of superimposed epochs, was used to study the effect of the geophysical activity on the physiological parameter up to three days before and three days after geomagnetic storms or CRI variations.

Day 0 is defined as the day the HR data were obtained. For this day, the geomagnetic and CRI activity were noted. According to the geomagnetic indices’ values and the CRI variations, the activity for each day was determined. For example, if for day 0 (the day HR data were obtained), the Dst index was greater than −100 nT and less or equal to −50 nT and the Ap index was less than 50 and greater or equal to 30, a strong geomagnetic storm was considered during this day (see Table 1). Similarly, for CRI, if for day 0 (the day HR data were obtained), CRI variations were −5%, a large Forbush decrease was considered. Moreover, days −3, −2 and −1 before the event correspond to the event’s initial phase and days +1, +2 and +3 after the event refer to the recovery phase of this event. Since both geomagnetic storms and Forbush decreases are events that their main phase lasts some hours, but their full development expands over a period of days [45,46], it is interesting to examine whether the physiological parameter HR presents notable variations not only during these events but also during the preparation and the restoration of the physical environment conditions.

3. Results

Before presenting the results of this work, it should be mentioned that this study continues and completes an investigation conducted by the Athens Cosmic Ray Group of the NKUA, involving medical data from different areas in the Greek region for the time interval April 2011 to January 2018 (covering solar cycle 24). HR data (1353 measurements) were evaluated during the aforementioned time period and the ascending and descending phases of the solar cycle 24. Detailed results were included in [47]. In summary, it was concluded that:

(1)

HR increase was observed for the highest levels of GMA (level IV of the Dst- and Ap index classification),

(2)

HR increase was observed during strong CRI decreases (i.e., decreases from −6% to −3%),

(3)

For levels III and IV of the GMA and strong CRI decreases, HR varied significantly on the days before (−), during (0), and after (+) the registered events,

(4)

p-values showed that HR is statistically significantly affected by GMA during the days before the geomagnetic storm and by CRI variations during the day of the event and the days after that,

(5)

HR was more susceptible to geophysical events during the ascending phase of solar cycle 24 (p-values showed that the GMA and CRI variations statistically significantly affected HR during the ascending and not the descending phase). This is because Forbush decreases, and geomagnetic storms are mostly displayed during and around the solar cycles’ maximum when intense solar activity is registered [48].

The daily variations of the Dst index (red dashed line), the Ap index (green punctuated line) and the CRI (blue dotted line) for the time interval under examination are shown in Figure 1. As mentioned, the strongest events are noticed around the maximum of solar cycle 24 (i.e., April 2014).

The significance levels (p) of the effect of the different levels of GMA and CRI on HR were calculated using the ANOVA method. The results concern the day of the event, the days before and after the geomagnetic storm, and the CRI variation. The significance levels (p) were estimated separately for the men and women of the database and are presented in

Table 2. Significance levels (p-values) of GMA and CRI potential effect on HR on the days before (−), during (0) and after (+) GMA and CRI variations.

p-Values
	Men			Women
Day	Dst	Ap	CRI	Dst	Ap	CRI
−3	0.60891	0.00814 *	0.42217	0.03582 *	0.97250	0.62050
−2	0.97030	0.54366	0.37163	0.31232	0.05227	0.60271
−1	0.29913	0.63379	0.26512	0.03914 *	0.00012 *	0.75154
0	0.87540	0.77509	0.23985	0.18530	0.52885	0.79933
+1	0.52118	0.29504	0.11402	0.64163	0.52075	0.57080
+2	0.40526	0.06567	0.34511	0.66130	0.37135	0.56819
+3	0.55468	0.29899	0.83225	0.34803	0.04097 *	0.78056

* Statistically significant results.

for the Dst and Ap indices and the CRI. It should be noted that no statistically significant results were obtained for the Dst index and CRI for men. Only the Ap index factor provided a statistically significant result on day −3. On the other hand, statistically significant results were acquired for women’s Dst- and Ap indexes on the days preceding and following geomagnetic storms. More precisely, the effect of the different levels of GMA on HR was noticed on days −3 and −1 (for the Dst index) and days −1 and +3 (for the Ap index). CRI, once again, did not provide statistically significant results. These findings confirm the alternative hypothesis that for the aforementioned days, GMA levels affect the physiological parameter HR.

The HR trend for both women and men for the defined different levels of GMA variations, i.e., Dst and Ap index and CRI fluctuations for Day 0, are presented in Figure 2, Figure 3 and Figure 4, respectively. In these figures, the two vertical axes correspond to the average HR values (in beats/min) for women (blue color, left axis) and men (red color, right axis), the horizontal axis denotes the different levels of GMA (see Section 2.3) and the CRI variations (in %) (see Section 2.2) and the vertical bars denote a 0.95 confidence interval. At this point, it should be stated that these figures present only an HR trend and not a definite behavior. Even though the HR trends discussed in the following are consistent with results presented in the international literature, a conservative approach to the results is preferred. This is due to the fact that statistically significant results for GMA and CRI variations were obtained only for certain days (see Table 2).

It is stated that human physiological parameters (HR, arterial blood pressure, psycho–physiological complaints, etc.) usually increase for high levels of geophysical activity [49]. In fact, higher HR values are observed for the highest GMA levels, i.e., levels III and IV of the Dst index classification, while small or even no variations are recorded for the lowest GMA levels, i.e., levels I0, I and II of the Dst index classification [42,47,50]. This behavior is observed in Figure 2 for women, where indeed the maximum HR value is registered for Dst index level IV, but not for men. For men, the HR variations were very small, i.e., HR was almost constant for levels I, II and II and decreased slightly for levels III and IV, where the minimum value was recorded [49].

Figure 2. HR aver (bpm) variations for the different levels of Dst index for Day 0 for women (blue line) and men (red line). The vertical bars denote a 0.95 confidence interval.

Figure 2. HR aver (bpm) variations for the different levels of Dst index for Day 0 for women (blue line) and men (red line). The vertical bars denote a 0.95 confidence interval.

On the contrary, for the Ap index (Figure 3), instead of the expected HR increase for severe GMA, HR maximum is observed for level II (moderate geomagnetic storms), and a decrease is observed from level II and there on until level IV. This behavior is evident in both men and women. Increased HR values during moderate GMA (as shown herein) are also reported in the literature [51]. For level IV, the HR minimum is recorded for men.

Figure 3. HR aver (bpm) variations for the different levels of Ap index for Day 0 for women (blue line) and men (red line). The vertical bars denote a 0.95 confidence interval.

Figure 3. HR aver (bpm) variations for the different levels of Ap index for Day 0 for women (blue line) and men (red line). The vertical bars denote a 0.95 confidence interval.

Furthermore, the results for CRI levels (Figure 4) are also noteworthy. For women, the maximum HR value is observed for moderate decreases of −3%. For the strongest decreases (−6%, −5% and −4%), HR has reduced values but stays almost constant, while for smaller CRI decreases and increases, HR decreases until the minimum value (for CRI increases +3%). For men, the behavior is basically similar, with slight differences in the strongest increases and decreases of the CRI. That is, the maximum HR is once again observed for CRI decreases of −3% and HR is reduced for either strong or minor decreases/increases. However, for CRI decreases of −6% and CRI increases of +3%, the HR increases. Similarly, CRI results for both men and women agree with the findings presented in [52].

Figure 4. HR aver (bpm) variations for the different CRI variations for Day 0 for women (blue line) and men (red line). The vertical bars denote a 0.95 confidence interval.

Figure 4. HR aver (bpm) variations for the different CRI variations for Day 0 for women (blue line) and men (red line). The vertical bars denote a 0.95 confidence interval.

As a general remark, it can be said that an obvious difference in HR behavior for men and women is marked for the Dst index. Especially for level IV of the GMA, HR had a maximum and a minimum value for women and men, respectively. Additionally, for extreme CRI variations (−6% decreases and +3% increases), the HR increased and decreased for men and women, respectively. For the Ap index, the HR for men and women behaved similarly.

Heart rate variations during the development of a geophysical event are depicted in Figure 5, Figure 6 and Figure 7. Therein, HR variations are presented for the three days before (days −3, −2 and −1), the day during (day 0) and the three days after (days +1, +2 and +3) geomagnetic storms and CRI variations. In these diagrams, each colored line represents the activity of the different levels of geomagnetic and cosmic rays.

Heart rate variations during GMA, expressed by the Dst index, are shown in Figure 5a for men and Figure 5b for women. As shown for men (Figure 5a), no significant HR variation was noticed for low levels of GMA, i.e., levels I0, I and II (blue, red and green lines, respectively). On the other hand, for the two higher levels of GMA, HR had peak values for the days before and after the day of the event, which is supported by previous results [47,49]. More precisely, for level III (pink line), HR got its maximum value on day −1 before the event and decreased until day 0 of the storm. HR got a minimum value on day +3 after the event. An opposite behavior was noticed for level IV (black line). HR had a minimum value on day −1 before the event and increased from there until day +1 after the event when the maximum was observed.

Figure 5. GMA effect (Dst index) on HRaver (bpm) for the days before, during, and after geomagnetic variations and for quiet levels for men (a) and women (b).

Figure 5. GMA effect (Dst index) on HRaver (bpm) for the days before, during, and after geomagnetic variations and for quiet levels for men (a) and women (b).

For women, results are shown in Figure 5b. Even though no significant HR variation is observed for levels I and II, for level I0, i.e., quiet period, HR varies during the event. This agrees with results claiming that small or even the absence of geomagnetic field variations may affect human health [53,54]. From the maximum value on day −3 before the event, HR decreases to the minimum value on day 0 and increases until day +2 after the event. For levels III and IV, women’s HR behavior is similar to that of men.

Furthermore, Ap index results are presented in Figure 6a for men and Figure 6b for women. As seen in Figure 6a, level I0 is almost constant, i.e., men do not respond to minor or no GMA. The same stands for levels I and II. For level III, the only noticeable behavior is that HR varied after the event (minimum value on day +2 after the event). On the other hand, level IV presented the most important variations. HR decreased from a maximum value on day −3 to a minimum value on day −2 before the event and had peak values during the following days.

Figure 6. GMA effect (Ap index) on HRaver (bpm) for the days before, during, and after geomagnetic variations and for quiet levels for men (a) and women (b).

Figure 6. GMA effect (Ap index) on HRaver (bpm) for the days before, during, and after geomagnetic variations and for quiet levels for men (a) and women (b).

The opposite behavior is recorded for women for the highest levels of GMA, expressed by the Ap index (Figure 6b). For example, for level III, HR varied significantly on the days before the geomagnetic storm (maximum on day −1 before the event). For level IV, unlike men, women’s HR increased from day +2 (minimum) until day +3 after the event (maximum).

Figure 7a,b shows HR variations during the development of CRI variations for men and women, respectively. For men, the HR variations are more pronounced for CRI, decreasing from −5% to −3% (Figure 7a). For CRI decreases of −5%, HR has peak values on the days before and after the CRI decrease. For CRI decreases of −4%, HR presented the largest variation (from 52 bpm to 75.4 bpm). For CRI decreases of −3%, HR increases from day −3 until day +1 after the event and decreases from thereon.

Concerning women, results show HR’s behavior (peak values) for CRI increases +3% (dark blue line), which is worth mentioning (Figure 7b). The peak values were recorded on the days before the CRI increase until day 0 of the CRI increase. This is not seen for men. Moreover, for CRI decreases of −5%, women’s HR behavior is similar to men’s (decrease on the days before the event until day 0, when HR minimum is observed and increase to a maximum value on day +1 after the event). On the other hand, for CRI decreases of −4% and −3%, women’s and men’s HR behavior are the opposite. On day −1 before the event, HR had a minimum value for men but a maximum value for women. Furthermore, for CRI decreases of −3%, men’s HR gets a maximum value on day +1 after the event, while for women, HR gets a minimum value on day +2 after the event.

Figure 7. CRI effect on HRaver (bpm) for the days before, during, and after CRI variations and for quiet levels for men (a) and women (b).

Figure 7. CRI effect on HRaver (bpm) for the days before, during, and after CRI variations and for quiet levels for men (a) and women (b).

As a general remark, it can be said that the analysis of HR variations during the development of geomagnetic storms and CRI variations showed that the most significant HR variations are mainly noticed for the highest levels of geophysical activity for both men and women, which is in accordance with previous results. Moreover, it was noted that women tend to be more susceptible to minor or no geophysical activity than men. In addition, HR’s behavior for men and women would coincide (e.g., for Dst index) or be opposite (e.g., for Ap index and CRI variations). The latter means that HR variations for men and women are either of opposite signs (increase/decrease) or of different temporal distribution concerning day 0 when the event was registered (variations recorded before or after the geomagnetic storm or the CRI variation).

4. Conclusions and Discussion

Space weather can potentially influence the physiological state of the human organism. This statement is supported by findings in various scientific studies [55,56,57,58,59]. Significant changes in HR were noticed from 1 to 3 days before significant fluctuations in the Ap and Dst indices and CRI variations. Thus, the effect precedes the cause. This observation is confirmed by various studies that state that numerous physiological parameters react to physical activity in the vicinity of ~2 days around the onset of physical events [13,32]. For example, it is presented in [49] that arterial blood pressure increased from day −2 before moderate, major and severe geomagnetic storms until day +2 after the event.

Moreover, [60] studied the electrical conductivity of biologically active points in relation to geomagnetic field variations. Therein, it was argued that the organs and systems of the individuals under investigation hyperfunctioned for almost 2 days around the onset of the geomagnetic storm. Additionally, it was reported that reactions due to stress, evaluated either by an electro-acupunctural experiment or by medical statistics, took place 1 to 2 days before a geomagnetic storm, by 49% and 30%, respectively [61,62].

Possible mechanisms on how heliogeophysical processes could directly or indirectly affect human physiology and health is a challenging subject that raises discussion. However, mechanisms mostly related to melatonin and the Schumann resonance have been proposed [53,63,64,65,66].

In general, variations of the physiological parameters, of HR in this case, could be explained by a probable, bio-physical mechanism that connects the solar, geomagnetic, and cosmic ray activity to human health and biological reactions. This mechanism is based on the effects of geomagnetic activity on the Earth’s electric and magnetic fields. Moreover, the precursory signs preceding geomagnetic and CRI activity could be responsible for provoking such sufficient reactions of the physiological parameters a few days prior to the main phase of events.

It is known that every biological system on Earth is exposed to either external or internal fluctuating electromagnetic fields with frequencies ranging from 0.1 to 10 Hz [53,66,67]. Moreover, after recording geoeffective phenomena occurring in the Sun and during the days before the development of a geomagnetic storm or an FD, extremely low-frequency fluctuations of the electromagnetic field occur. These fluctuations are classified as Pc1 (frequency range 0.2–5 Hz), Pc2 (0.1–0.2 Hz), Pc3 (22–100 mHz), Pc4 (7–22 mHz), and Pc5 (2–7 mHz) [10].

Several organs of the human body and systems (bioelectric waves of the human brain, cardiac rhythm, etc.) have frequencies close to those mentioned above [49]. For example, the heart’s rhythm frequency of oscillations is 2–5 Hz, i.e., in the same frequency range as Pc1–Pc5. A resonance effect on these extremely low-frequency fluctuations on the physiological state of the human organism is possible. As a result, a disturbed environment can impact the physiological state of humans [64].

This investigation focuses on the effect of geomagnetic disturbances and CRI variations on the HR of men and women. The data were provided by three hospitals in the region of Greece (Athens, Piraeus, and Heraklion) and expanded from April 2011 to January 2018, i.e., covering solar cycle 24. Geomagnetic data (Dst index and Ap index) and CRI data were also evaluated.

The most interesting results of this study, separated by sex, are highlighted in

Table 3. Results separated by sex.

Male Sex	Female Sex
p-values
(1) Statistically significant results were acquired for geomagnetic index Ap three days before geomagnetic storms.	(1) Statistically significant results were acquired for the geomagnetic Ap index one day before and three days after the geomagnetic storm.
(2) No statistically significant results were obtained for geomagnetic index Dst.	(2) Statistically significant results were acquired for the geomagnetic Dst index one day and three days before the geomagnetic storm.
(3) No statistically significant results were obtained for CRI.	(3) No statistically significant results were obtained for CRI.
For different levels of geomagnetic and cosmic ray activity
(4) For the geomagnetic Dst index, severe geomagnetic storms (level IV) were connected to an HR decrease.	(4) For the geomagnetic Dst index, severe geomagnetic storms (level IV) were connected to an HR increase.
(5) For the geomagnetic Ap index, the maximum HR value was recorded for level II (moderate GMA). High GMA levels (levels III and IV) were connected to low HR values.	(5) For the geomagnetic Ap index, the maximum HR value was recorded for level II (moderate GMA). High GMA levels (levels III and IV) were connected to low HR values.
(6) For the CRI variations, the maximum HR value was recorded for CRI decreases of −3%. For stronger CRI decreases and minor CRI decreases or CRI increases, HR had reduced values.	(6) For the CRI variations, the maximum HR value was recorded for CRI decreases of −3%. For stronger CRI decreases and minor CRI decreases or CRI increases, HR had reduced values.
During the development of an event
(7) Regarding the geomagnetic Dst index, for low levels of GMA, i.e., levels I0, I and II, no significant HR variations were noticed.	(7) Regarding the geomagnetic Dst index, for level I0 (quiet period), HR varies during the event.
(8) Regarding the geomagnetic Dst index, for levels III and IV, HR had peak values on the days before and after the day of the event.	(8) Regarding the geomagnetic Dst index, for levels III and IV, HR had peak values on the days before the day of the event.
(9) Regarding the geomagnetic Ap index, for low levels of GMA, i.e., levels I0, I and II, no important HR variations were noticed.	(9) Regarding the geomagnetic Ap index, for low levels of GMA, i.e., levels I0, I and II, no important HR variations were noticed.
(10) Regarding the geomagnetic Ap index, for the highest level of GMA, i.e., level IV, the HR maximum and minimum values were recorded the days before the event.	(10) Regarding the geomagnetic Ap index, for the highest level of GMA, i.e., level IV, the HR maximum and minimum values for women were recorded the days after the event.
(11) Regarding CRI, the HR variations are more pronounced for CRI decreases from −5% to −3%.	(11) Regarding CRI, the HR variations are more pronounced for CRI decreases from −5% to −3%.
(12) Regarding CRI, for CRI decreases of −4%, HR has a minimum value one day before the event. For a CRI decrease of −3%, HR gets the maximum value one day after the event.	(12) Regarding CRI, for CRI decreases of −4%, HR has a maximum value one day before the event. For CRI decreases of −3%, HR gets a minimum value two days after the event.
	(13) Regarding CRI, HR for CRI increases of +3% is noticeable.

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It is argued that space weather phenomena can affect human health, with this effect being more pronounced for women. Many examples are mentioned in various studies in the international literature (e.g., [26]). For example, concerning arterial systolic and diastolic blood pressure, [68] showed that the impact of GMA variations daily is stronger on women than men. Similarly, occurrences of myocardial infarction are stronger in women in terms of heliophysical parameters [30]. Moreover, the authors of [69] claimed that geomagnetic storms occurring one day after hospital admission almost quadrupled the hazard ratio of cardiovascular death for women, making them more susceptible to heliophysical effects.

The results of this particular study, presented herein, are in accordance with the abovementioned argument. Therefore, HR variations may be another physiological parameter, amongst others, i.e., arterial blood pressure, myocardial infarctions, etc., that could act as an indicator and verify women’s high sensitivity to changes in the geophysical environment.

Human physiology is determined endogenously (stress, quality of life, nutrition, etc.) and exogenously [70]. For instance, meteorological weather can affect human health [71], as can exposure to radiation or chemical substances, etc. Separating the impact of each of these factors is a difficult problem to solve in heliobiological studies. This is why various investigations performed in different regions are important, as they provide reliable and collective results.

This work contributes considerably in this direction since it is part of a wider investigation conducted by the Cosmic Ray Group of the NKUA in collaboration with different scientific groups from Bulgaria, Azerbaijan, and Slovakia. In these studies, amongst other physiological parameters (such as arterial blood pressure and RR intervals), HR has been evaluated in regard to geophysical processes [23]. The parameters of HR have been analyzed in different geographical regions, during different time periods, and for different groups of individuals. Herein, a step further is taken, and HR is studied depending on sex. At this point, it should be highlighted that this research is an asset to the heliobiological studies since it provides, to the greatest extent, a complete study of the HR parameter in relation to GMA and CRI variations. The method of obtaining the HR data was the same in all studies (i.e., Holter electrocardiogram), as was the method of analysis. Therefore, it is possible to compare these findings and reach consistent results.