# Hypomagnetic Conditions and Their Biological Action (Review)

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## Abstract

**:**

## Simple Summary

## Abstract

## 1. Introduction

## 2. Experimental Approaches

^{3}[39,40]. The second approach is the use of active compensation of the geomagnetic field [36,41]. For this, a system of Helmholtz coils is used, usually three pairs, oriented along three orthogonal axes [35,40]. However, this can also be a single-axis option. In this case, the system axis is directed collinear to the geomagnetic field vector [42,43,44]. The coils generate a magnetic field oppositely directed relative to the geomagnetic field lines and close in induction values to the geomagnetic field induction. Thus, the resulting magnetic field in the internal section of the installation becomes “near zero”. The volume of space with a stable hypomagnetic field, in this case, depends on the size of the coils and, as a rule, ranges from 10 cm × 10 cm × 10 cm to 50 cm × 50 cm × 50 cm [32,34,43,45]. Particularly large installations used for research on humans can have a working volume of up to ~3 m

^{3}[43].

^{3}–10

^{4}times, and can reach values of <200 nT [49,50] (Figure 2). Compensation systems based on Helmholtz coils have comparable efficiency and allow compensation to be achieved down to resulting field induction values of up to 10 nT or below [44,51]. Recently, Helmholtz coils were used in most of the works. The magnetic field induction, in this case, was lower than in work with soft magnetic materials’ shielding chamber (Figure 2). Compensation of the variable magnetic field component in systems based on Helmholtz coils has its limitations. Thus, in the installation described in the works, a fluxgate sensor (high-sensitive three-axial sensor FL3-100, produced by Stefan Mayer Instruments, Dinslaken, Germany) is used [52,53]. Since the sensor bandwidth is limited to the frequency range 0 to 2 kHz (−3 dB), compensation of variable magnetic fields was only possible for low-frequency magnetic fields. At a frequency of 1 Hz, the compensation was 10

^{3}times, at 50 Hz, 8–10 times, and at a frequency of 500 Hz, compensation no longer occurred.

№ | Biological Object | Characteristics | Effect, % | Magnetic Flux Density | Time | N | Statistic | Validation | Experimental Setup | Size or Volume | SJR | Ref. |
---|---|---|---|---|---|---|---|---|---|---|---|---|

1 | Human, men and women, average age of 45 ± 18 years | Heartbeat rate (≥40 years) Heartbeat rate (<40 years) Diastolic blood pressure (under 40 years) Capillary blood flow rate | −20% +10–15% −4–5% +22–23% | 10 nT >> >> >> | 120 min >> >> >> | 32 >> >> >> | ANOVA, F-test | Magnetometer, 3-axis, spatial distribution, HMF variation < 10 nT GMF: ~48 μT, meteorological data were used to choose assay days | Helmholtz coils (3-axis) | 2.6 m^{3} | 0.42 (Q2) | [44] |

2 | Rat Rattus norvegicus adult | Number of erythrocytes (RBC), Hematocrit (EPV), Erythrocyte volume (MCV), Hemolysis | +12% +7% −10% −85% | 0.192 μT >> >> >> | 1–4 days >> >> >> | 3 >> >> >> | Student’s paired t-test | Magnetometer, 3-axis, 1 point | Shielding chamber from amorphous magnetic material AMAG-172 | - | - | [37] |

3 | Zebrafish Danio renio wild type (AB strain), embryos | Viability Heartbeat rate | −10% +5% | <300 nT >> | 120 h >> | 200 >> | Shapiro–Wilk W-test or Kolmogorov–Smirnov test, Levene’s test, t-test, Cosinor analysis (for circadian rhythms) | Magnetometer 3-axis spatial distribution GMF: 51.7 μT AFM: 50 Hz, < 15 nT without harmonics | Helmholtz coils (3-axis) | Ø 50 cm | 1.03 (Q1) | [48] |

4 | Human men (24–53 years) and women (26–49 years) | Higher nervous activity: test for matching the meaning of a word and its color: lead time error rate Letter recognition test: lead time error rate | +10% +15% +5% +150% | <0.4 μT >> >> >> | 1 h 17 min >> >> >> | 40 >> >> >> | Multivariate analysis of variance (MANOVA) | Magnetometer, 3-axis, spatial distribution, variation < 0.2 μT GMF: ~41 μT AMF variations complicated | Helmholtz coils | ~3 m^{3} | 0.4 (Q3) | [42] |

5 | Rat, Rattus norvegicus line Wistar | Open field testing: horizontal component, vertical component, general physical activity Power of EEG rhythms: Theta Alpha Beta Gamma | −20% −30% −50% −50% −50% −50% −50% | 50 nT >> >> >> >> >> >> | 21 days >> >> >> >> >> >> | 12 >> >> >> >> >> >> | Wilcoxon signed-rank test, Kolmogorov–Smirnov test | Magnetometer, 3-axis, 1 point, HMF variation: < 50 nT | Helmholtz coils (2-axis) | Ø 50 cm | - | [57] |

6 | Rat, Rattus norvegicus line Wistar | Number of aggression acts (day) Number of aggression acts (night) | +130% +17 times | 50–150 nT >> | 21 days >> | 12 >> | Wilcoxon signed-rank test, Kolmogorov–Smirnov test | Magnetometer, 3-axis, 1 point, HMF variation: < 50 nT | Helmholtz coils | Ø 50 cm | - | [58] |

7 | Golden hamster Ochrotomys nuttalli adults | Proportion of noradrenergic neurons in areas A3 and A7 of the brainstem | −29% −35% | 22 nT >> | 60 180 days | 5 >> | One-way ANOVA or Student’s t-test | Magnetometer 3-axis spatial distribution: 0.022–2.8 μT | Permalloy chamber | 70 cm × 70 cm × 90 cm | 0.42 (Q3) | [59] |

8 | Mice (M. musculus) C57BL/6 J adults, 8–10 weeks | Behavioral tests: Freezing in context test Freezing in cue test | −15% −12% | 170 nT >> | 8 weeks >> | 10 >> | One-way or two-way ANOVA or Student’s t-test | Magnetometer, 3-axis, spatial distribution, ambient magnetic fields, noise and light were measured. SMF in incubator: 39.4 ± 3.6 μT. AMF: 50 Hz Bt PSD1/2 2.37 nT/√Hz | Helmholtz coils (3-axis) | Ø 50 cm | 5.12 (Q1) | [60] |

9 | Mice, C57BL/6J, 7 weeks old | Open field behavior test: percent time spent in the center, total traveled distances, time spent exploring the novel location, time spent exploring a novel object | −80% 0% −30% −30% | 31.9 nT >> >> >> | 8 weeks >> >> >> | 10 >> >> >> | Double-blind study, unpaired Student’s t-test | Magnetometer 3-axis 1 point, time distribution, HMF variation: < 4.5 nT GMF: ~55 μT temperature, illumination, and relative humidity equal in all conditions | Helmholtz coils (3-axis) | 2 m × 2 m × 2 m | 1.15 (Q1) | [61] |

10 | Chicken Gallus gallus domesticus incubated in hypomagnetic conditions, eggs and chicks hatched from them | Retained curve in one-trial passive avoidance task (OTPAT) Temporary mean memory test Long-term memory test | −68.4% −74.8% | 354 nT >> | 21 days >> | 10 >> | One-way ANOVA | Magnetometer, 1-axis, 1 point HMF variation: < 254 nT | Helmholtz coils (3-axis) | Ø 120 cm | 1.45 | [62] |

11 | Fruit fly Drosophila melanogaster imago, females 3–4-diurnal Prussian wild type (10–19 successive generations) | Performance index (PI) of operant visual learning and memory (L/M) formation of flies | −65% | 100–680 nT | 40–80 days | 445 | One-way ANOVA | Magnetometer, 1-axis, spatial distribution, GMF: 52.21 μT | Helmholtz coils (3-axis) | 50 cm × 50 cm × 50 cm | 0.8 (Q2) | [63] |

12 | Brown planthopper, Nilaparvata lugens males and females, imago | Direction of movement in food (decrease transition to random movement) | −100% | ~500 nT | 24–48 h | 500 | Student’s t-test | Magnetometer, 3-axis, spatial distribution (homogeneity HMF at Ø 150 mm) GMF: 52.5 ± 0.8 μT | Helmholtz coils (3-axis) | Ø 15 cm | 0.7 (Q1) | [64] |

13 | Oriental armyworm, Mythimna separata, adults, males and females | Flight spatial orientation | −100% | 500 nT | 20 s | 9 | Rayleigh’s test, Watson–Williams test | Magnetometer, 3-axis, 3D map, HMF variation: < 4% | Helmholtz coils | Ø 120 cm | 0.82 (Q1) | [65] |

14 | Black Garden Ant (Lasius niger) | Behavior: Time to reach food, Time to return to the nest, Mistakes to reach food | +200% +40% +300% | ~40 nT >> >> | 14 days >> >> | 1000 >> >> | Kolmogorov–Smirnov test, one-way ANOVA, Tukey’s post hoc test | Magnetometer, 3-axis, spatial distribution, HMF variation: < 6 µT GMF: ~42 µT GMF variation: <20 nT | Helmholtz coils (3-axis) | Ø 128 cm | 1.15 (Q1) | [66] |

15 | Brown planthopper, S. furcifera, males and females, imago | Positive phototaxis Speed, duration, and range of flight Body weight | −20% −40% −8% | ~477 nT >> >> | 1–5 days >> >> | 40 >> >> | One-way or two-way ANOVA | Magnetometer, 1-axis, spatial distribution (0–1.06 μT) GMF: ~50 μT | Helmholtz coils (3-axis) | Ø 30 cm | 0.74 (Q1) | [45] |

16 | Rat (Rattus norvegicus) Wistar line, females and males | Concentration of Fe, Mn, Co, Ni, Cr, Cu in hair | −5–40% (depending on the element and sex of the animal) | <20 nT | 7 months | 8 | One-way ANOVA | Magnetometer 1-axis 1 point | Chamber from steel type S235JRG2 | ~1 m × 1 m × 1 m | 0.94 (Q1) | [29] |

17 | Fishes, 0–1 year, Carassius carassius, Rutilus rutilus, Cyprinus carpio, snail Limnaea stagnalis, planktonic crustaceans, Daphnia magna (imago) | The concentration of Fe, Mn, Co, Ni, Cr, Cu in the brain, skeletal muscles (fishes), or all organisms (daphnia) | −50 % (depending on the element, organ, and species) | <10 nT | 1 h | 7 | Mann–Whitney test | Magnetometer 1-axis 1 point GMF: 51.7 μT | Helmholtz coils (3-, 1-axis) | Ø 50 cm | 0.31 (Q3) | [67] |

18 | Brown planthopper, Nilaparvata lugens migrating adults, eggs | Body weight of hatched insects Body weight of 5th instar nymphs Feeding of 5th instar nymphs Glucose content in 5th instar nymphs | 15% −35% −35% +20% −15% | 480 nT >> >> >> >> | 48 h >> >> >> >> | 20 >> >> >> >> | Shapiro–Wilk test, Levene’s test, one-way ANOVA, or Mann–Witney U-test | Magnetometer, 1-axis, spatial distribution, HMF variation: < 5% GMF: ~50 μT | Shielding chamber from μ-metal alloy and Helmholtz coils (3-axis) | Ø 30 cm | 0.94 (Q1) | [68] |

19 | Rat Rattus norvegicus line Sprague Dawley 250–270 g | Body weight Strength characteristics of bones: Ultimate Power Hardness factor Elastic modulus Density Weight Number of trabeculae Degree of bone anisotropy concentration of receptor activator of nuclear factor-kB ligand (RANKL) in bone tissue Serum: Concentrations of bALP, DPD, and GCs | −17% −18% +18% +17% −18% −15% +50% −25% −75% +35% | <300 nT >> >> >> >> >> >> >> >> >> | 28 days >> >> >> >> >> >> >> >> >> | 30 >> >> >> >> >> >> >> >> >> | One-way or two-way ANOVA | Magnetometer, 1-axis, 1 point GMF: ~50 µT, illumination and ventilation conditions as HMF and GMF were equal | Shielding chamber (aluminum/permalloy/silicone/iron) | 1.86 m × 1.66 m × 1.5 m | Rat (Rattus norvegicus) line Sprague Dawley, 250–270 g | [69] |

20 | Mice, males C57BL/6 hindlimb suspension model | Bone mineral content, Ultimate bending moment, Ultimate stress, Bone volume fraction, Trabecular separation, Connectivity density, Osteoblast number, Osteoclast number, Osteoclast surface, Bone eroded surface, Serum levels of tartrate- resistant acid phosphatase (bone resorption marker) Serum iron, Ferritin level Total iron content: liver, spleen Bone iron, Bone marrow iron | −20% −15% −15% −40% +15% −40% −40% +30% +15% +30% +20% +30% +20% +20% +35% +20% +20% | <300 nT >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> | 4 weeks >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> | 6 >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> | Two-way ANOVA, Sidak’s post hoc test | Magnetometer, spatial distribution, AMF in control incubator 50 Hz ~1 μT AMF in an experimental incubator 50 Hz, < 12 nT GMF: ~45 μT | Permalloy chamber | 550 m × 420 m × 420 m | 1.13 (Q1) | [70] |

21 | Mouse M. musculus line NMRIz, pregnant females, embryos 3 days after fertilization | Birth rate, Number of implanted embryos, Histological abnormalities, resorption | −30% −30% +Qualitatively | <200 nT >> >> | 12 days >> >> | 5 >> >> | Student’s t-test | Magnetometer, 1-axis, 1 point, GMF: ~40 μT | Permalloy chamber | - | 0.4 (Q3) | [71] |

22 | Brown planthopper S. furcifera eggs and nymphs | Body weight (2 days old): Female, Male Positive chemotaxis: Females (5 days old), Males (2 days old), Males (5 days old) Flight speed (2 days old): Females, Males Flight duration: Female, Male Flight distance: Female, Male | −5% −10% +40% +30% +30% +30% −20% −80% +40% −60% N/A | 477 nT >> >> >> >> >> >> >> >> >> >> | 2000 h >> >> >> >> >> >> >> >> >> >> | 40 >> 115 >> >> 23 46 23 46 23 46 | Two-way ANOVA, MANOVA, Shapiro–Wilk test (normality), chi-square test (two-tailed) with Yates’s correction, Student’s t-test | Magnetometer, 3-axis, one point, HMF variation: < 25 nT GMF: ~52 μT, temperature variation: < 0.1 °C | Helmholtz coils | Ø 120 cm | 1.04 (Q1) | [72] |

23 | Oriental armyworm; Mythimna separata eggs, larvae, pupae, and imago (females and males) | Duration of development stages: larval doll imago (males) Pupa mass Number of eggs laid by one female | +5% +2% +5% −20% −5% −45% | <500 nT >> >> >> >> >> | 12 h >> >> >> >> >> | 300 >> >> >> >> >> | One-way or two-way ANOVA | Magnetometer, 1-axis, 1 point, time distribution, HMF variation: < 500 nT | Helmholtz coils | Ø 50 mm | 0.94 (Q1) | [73] |

24 | Crustaceans, Daphnia magna Daphnia carinata newborns and adults | Newborn sizes Adult sizes Life length | −15% −5% −5% | <15 nT >> >> | 24 h >> >> | 30 >> >> | Kolmogorov–Smirnov test, Levene’s test (homoscedasticity), one-way analysis of variance (ANOVA), Dunnett’s post hoc test | Magnetometer, 3-axis, spatial distribution AFM: 50 Hz < 12 nT GMF 51.7 mT | Helmholtz coils (3-axis) | Ø 50 cm | 0.4 (Q3) | [74] |

25 | Human men and women (<40 years) | Pupil diameter | +1.6% | 300–600 nT | 40 min | 40 | One-way ANOVA | Magnetometer, 3-axis, spatial distribution, variation: < 0.4 μT GMF: ~41 μT AMF variations complicated | Helmholtz coils | 1 m × 1 m × 1.5 m | - | [75] |

26 | Tardigrades (Paramacrobiotus experimentalis) females and males of different age | Proportions of active animals | −10% | <250 nT | 7 days | 45 | two-way ANOVA, Tukey post hoc test | Magnetometer 1-axis 1 point GMF: ~50 μT | μ-Metal shielding chamber (approximately 77% nickel, 16% iron, 5% copper, and 2% molybdenum) | 18.5 cm × 12 cm × 33 cm | 1.03 (Q1) | [76] |

27 | Helix albescens large common snail | Duration of circadian rhythms | −17% +19% | 0.5–2 µT >> | 3 days 21 days | 20 >> | Fourier transformation, Student’s t-test (normality tested) | Magnetometer, 1-axis, 1 point, spectral density of magnetic noise: < 10 nT/Hz | Room covered with Dynamo iron leaves | 2 m × 3 m × 2 m | 1.07 (Q1) | [77] |

28 | Tardigrades Echiniscus testudo and Milnesium inceptum | Mortality rate: (1) dehydrated (2) during dehydration (3) returning to active life after dehydration | +45% +80% +200% | <25 nT >> >> | 21 days >> >> | 100 >> >> | One-way ANOVA, Tukey test as a post hoc test, or Student’s t-test with the Cochran–Cox adjustment | Magnetometer, 1-axis, 1 point GMF: ~50 GMF | Shielding chamber amorphous magnet (μ-metal) | 18.5 cm × 12 cm × 33 cm | 0.7 (Q1) | [38] |

## 3. Effects of HMC on Living Objects

#### 3.1. Effects of HMC on Animals (Organ and Organism Level)

#### 3.1.1. Nervous System

#### 3.1.2. Cardiovascular System and Immunity

#### 3.1.3. Musculoskeletal System, Metabolism, and Other Effects

#### 3.2. Effects of HMC on Plants

_{3}

^{+}, K

^{+}, Ca

^{2+}, and Mg

^{2+}) and anions (Cl

^{−}, SO

_{4}

^{2−}, NO

_{3}

^{−}, and PO4

^{−3}) via an increase in the expression of Ca

^{2+}and Mg

^{2}cation and Cl

^{−}, SO

_{4}

^{2−}, NO

_{3}

^{−}, and PO4

^{−3}anion transporter proteins [92]. In addition, HMCs reduce the expression of regulators of circadian rhythms and floral meristem growth [90]. Using peas as an example, HMCs cause an increase in osmotic pressure in the roots of seedlings [93]. It has been shown that HMCs cause an increase in the concentration of the stress hormone gibberellin in plants and the launch of stress-activated signaling cascades [31]. An unobvious effect of HMC is a significant (two-fold) increase in the expression of proteins that regulate the response to light (cryptochrome A and phytochrome A) and a decrease in the expression of phytochrome B [94]. Activation of the phytochrome system enhances auxin synthesis in roots and reduces it in above-ground parts, changes the regulation of auxin-induced genes, enhances root growth, and inhibits stem growth; as a result, plants acquire rosette morphology [95,96]. The authors suggest that plant phytochrome signaling systems are involved in the response of plants to HMC [94]. Other studies have shown that HMC causes a redistribution of the concentrations of photosynthetic pigments in lima bean leaves, and also reduces the formation of ROS (H

_{2}O

_{2}) due to an increase in the expression of antioxidant enzymes [97]. These data may shed light on possible complications with the cultivation of plants onboard space stations of the future and possible ways to overcome them.

№ | Biological Object | Characteristics | Effect, % | Magnetic Flux Density | Time | N | Statistic | Validation | Experimental Setup | Size or Volume | SJR | Ref. |
---|---|---|---|---|---|---|---|---|---|---|---|---|

1 | Arabidopsis thaliana seedlings, WT and spl7-KO | Fe uptake by roots, Zn uptake by roots, Expression of Fe-deficiency-induced genes in roots: IRT1, AHA2, FIT, ILR, bHLH38, bHLH39, 3, FRO2, Spl7 knockout or Fe supplementation alters hypomagnetic condition effects | −2 times −2 times +2–10 times −2–3 times | ~40 μT >> >> >> | 96 h >> >> >> | 4 >> 3 >> | One-way ANOVA | Magnetometer, 3-axis, spatial distribution, GMF: 41–43 μT | Helmholtz coils (1-axis) | - | 1.23 (Q1) | [91] |

2 | Arabidopsis thaliana Landsberg erecta, wild type, seedlings | Hypocotyl lengths: blue light, darkness | −3% +6% | ~10 nT >> | 72 h >> | 30 >> | Paired t-test | Magnetometer, 1-axis, 1 point SMD variation: < 10 μT GMF: ~50 mT | Helmholtz coils (1-axis) | Ø 22 cm | 1.2 (Q1) | [98] |

3 | Arabidopsis thaliana, wild type and spl7, amiFRO5, and amiFRO4/5 mutant lines | Fe concentration: control S index: S deficit Shoot area: control, Fe deficit Root length: control, Fe deficit, S deficit, Fe and S deficit Gene expression (part): AHA (Fe deficit), FRO (Fe and S deficit), PYE (Fe deficit), bHLH38 (Fe and S deficit) | −25% −20% −5% −5% −10% −10% −10% −10% −55% +45% −50% +50% | 42 nT >> >> >> >> >> >> >> >> >> >> >> | 7 days >> >> >> >> >> >> >> >> >> >> >> | 3 >> >> >> >> >> >> >> >> >> >> >> | Two-way ANOVA, Tukey’s post hoc test | Magnetometer, 3-axis, time distribution, variation: < 2nT, GMF: 41–43 μT | Helmholtz coil (3-axis) | Ø 128 cm | 1.15 (Q1) | [99] |

4 | Lima bean (Phaseolus lunatus) seeds and seedlings | Tomato leaf density, leaf area, relative water content, the major axis of chloroplast length, total carbohydrate content, total protein content, percentage of leaf carbon, carbon isotope discrimination (δ13C) Concentrations: Chlorophyll a, Chlorophyll b, Chlorophyll a’, Chlorophyll b’, Pheophytin a, Lutein, Trans-α-carotene, cis-α-carotene, Trans-β-carotene, 9-cis-β-carotene Protein expression: catalase, ascorbate peroxidase, peroxidase, glutathione reductase, glutathione peroxidase ROS production: peroxide, H _{2}O_{2} | +50% −30% N/A +20% −20% +10% +5% +30% −20% −20% +250% +100% +100% −40% −30% −25% −75% −40% −25% −2500% +10% −200% +200% +500% −75% −10% | ~40 nT >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> | 96 h >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> | 3 >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> | Paired Student’s t-test and Bonferroni post hoc test | Magnetometer, 3-axis, time distribution, variation: < 2 nT GMF: 41.94 μT | Helmholtz coil (3-axis) | Ø 128 cm | 1.15 (Q1) | [97] |

5 | Arabidopsis thaliana ecotype Landsberg erecta, WT or cry1cry2 mutants | Photosynthesis gene expression: rbcl (ribulose 1,5 bisphosphate), cab4 (chlorophyll a,b binding protein), pal4 (phenylalanine ammonia lyase), ef1 (elongation factor-1) | −20% −60% −20% −5% | 0.2 μT >> >> >> | 120 h >> >> >> | 4 >> >> >> | Student’s t-test | Magnetometer, 3-axis, spatial distribution, power supplies were separated from the μ-metal cylinder GMF: ~38 μT | Faraday-cage room, Helmholtz coils (2-axis) | 5.04 × 2.04 × 2.1 m Ø 18 cm | 0.88 (Q1) | [100] |

6 | Arabidopsis thaliana ecotype Col0, seedlings | Expression of circadian rhythm regulator genes: LHY, PRR7, GI | −80% −80% +60% | ~40 nT >> >> | 7 days >> >> | 3 >> >> | Two-way ANOVA, Tukey post hoc test | Magnetometer, 3-axis, spatial distribution, GMF: 40–45 μT | Helmholtz coil (3-axis) | - | 0.88 (Q1) >> | [101] |

7 | Arabidopsis thaliana (Col-0), Wt and cry1cry2-, phot1-, phyA-, and phyAphyB-deficient mutants, seedlings (1 week) | Changes in cryptochrome expression in response to blue light: Wt, phyA mutant Changes in phyA (phytochrome A) expression in response to red light Changes in cryptochrome expression in response to red light | +100% −100% −100% | ~40 nT >> >> | 96 h >> >> | 3 >> >> | Kolmogorov–Smirnov test (normality), one-way ANOVA, Tukey, and Bonferroni post hoc tests | Magnetometer, 3-axis, spatial distribution, sample rate: 10 s | Helmholtz coil (3-axis) | - | 0.87 (Q1) | [94] |

8 | Soy Glycine max seeds and seedlings | Gravitropism angle, Radicle weight ratio, Germination percentage, Germination rate, A ratio of root length to seed length | −50% +18% N/A −10% +12% | <111 nT >> >> >> >> | 1 h >> >> >> >> | 10 >> >> >> >> | Two-way ANOVA | Magnetometer 3-axis 1 point Temperature and relative humidity equal in both conditions | Chamber from 12 layers of permalloy sheets, enclosed within an outer aluminum layer | ~10 cm × 10 cm × 10 cm | 0.6 (Q2) | [88] |

9 | Arabidopsis thaliana ecotype Columbia | Epicotyl length, Adult habitus-acquisition of rosette morphology, Expression of phytochrome B signaling pathway genes: PHYB, CO, FT | +30% qualitatively −40% −40% −50% | <50 nT >> >> >> >> | 36 days >> >> >> >> | 20 3 >> >> | Student’s t-test | Magnetometer, 3-axis, spatial distribution, GMF: ~45 μT | Helmholtz coil (axis) | Ø 88 cm | 0.6 (Q2) | [96] |

10 | Arabidopsis thaliana Adult | Biomass (total) Biomass (dry) Flowering time Number of fruits per plant Seed weight per plant Harvest index (ratio between seed weight and total biomass) | −30% −40% +5% −20% −20% −20% | <1 μT >> >> >> >> >> | 35 days >> >> >> >> >> | 20 >> >> >> >> >> | One-way ANOVA | Magnetometer, 3-axis, 3D map GMF: ~42 μT HMF variation: < 50 nT | Helmholtz coil (3-axis) | Ø 80 cm | 0.43 (Q3) | [89] |

11 | Arabidopsis thaliana (Col-0), Wt | Time from germination to flowering, Time from germination to fruiting, Restoration of characteristics above after change in hypomagnetic condition to geomagnetic Leaf area index, Stem length, Expression of clock genes and photoperiod pathway genes, Expression of floral meristem genes, Expression of GA20ox2 | +20% +15% +100% −15% −30% −1.5–2.2 times −3–5 times −50 times | 41 nT >> >> >> >> >> >> >> | 15 min >> >> >> >> >> >> >> | 15 >> >> >> >> >> >> >> | Kolmogorov–Smirnov test, one-way ANOVA | Magnetometer, 3-axis, time distribution, variation: < 2 nT GMF: 41.94 μT | Helmholtz coil (3-axis) | Ø 128 cm | 0.43 (Q3) | [90] |

12 | Arabidopsis thaliana ecotype Columbia Col-4 Adult WT cry1-/cry2-mutants | WT: Expression of GA3ox1, Expression of GA3ox2, Expression of GA3ox3, LFY, SOC1, Gibberrilin concentration cry1-/cry2-mutants: Expression of GA3ox1, Expression of GA3ox2, Expression of GA3ox3, Gibberrilin concentration | −45% −55% −55% −35% −30% ~50% - 0 0 0 | <1 μT >> >> >> >> >> >> >> >> | 33 days >> >> >> >> >> >> >> | 3 >> >> >> >> >> >> >> | One-way ANOVA | Magnetometer, 3-axis, spatial distribution, GMF: ~45 μT | Helmholtz coil (3-axis) | Ø 88 cm | 0.42 (Q3) | [31] |

13 | Arabidopsis thaliana ecotype Columbia Col-4 Adult WT cry1-/cry2-mutants | WT: Auxin Levels in leaves, Auxin Levels in roots, Expressions of Auxin Transporter Genes, Expressions of Auxin Signaling Genes cry1-/cry2-mutants: Inhibition of the hypomagnetic field effects | −25% +40% +20% +30% 0 | <1 μT >> >> >> >> | 33 days >> >> >> >> | 3 >> >> >> >> | One-way ANOVA | Magnetometer, 3-axis, spatial distribution, GMF: ~45 μT | Helmholtz coil | Ø 20 cm | 0.42 (Q3) | [95] |

14 | Arabidopsis thaliana adult, wild type | Cation content in roots: NH _{3}^{+},K ^{+},Ca ^{2+},Mg ^{2+}Gene expression: Ca ^{2+}-transporting ATPase 11,Mg ^{2+} transporter CorA-like protein-relatedAniom content in roots: Cl ^{−},SO _{4}^{2−},NO _{3}^{−},PO4 ^{−3},Gene expression: Cl ^{−} channel protein (CLC-A),Cl ^{−} channel protein (CLC-C),Cl ^{−} channel protein (CLC-G),SO _{4−} transporter (Sultr3;1),NO _{3}^{−} transporter (NRT1.6),NO _{3}^{−} transporter (NRT2.4),PO _{4}^{3-} transporter (PHT1;8) | +25% +5% −15% +5% +50% −5% −15% −10% −50% +80% −10% +40% −90% +30% +8% −15% +10% −30% +2% +15% +60% −5% −40% +90% −80% +30% −30% +5% +8% −40% +5% +5% −50% −10% +5% −50% +15% −12% −25% +10% −15% −25% −10% −15% −3% −11% −3% +43% +46% +46% | <33 nT >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> | 1 h 4 h 24 h 48 h 10 min 1 h 4 h 48 h 96 h 10 min 4 h 48 h 96 h 10 min 1 h 4 h 24 h 96 h 4 h 48 h 10 min 1 h 4 h 48 h 96 h 10 min 4 h 24 h 48 h 96 h 10 min 1 h 4 h 24 h 48 h 96 h 10 min 1 h 4 h 24 h 48 h 96 h 1 h 4 h 1 h 96 h 1 h 48 h 48 h 48 h | 3 >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> >> | Paired Student’s t-test, and Bonferroni post hoc test, and Hochberg (BH) multiple testing correction | Magnetometer, 3-axis, spatial distribution, GMF: 41.94 μT | Helmholtz coils (3-axis) | Ø 128 cm | 0.41 (Q2) | [92] |

15 | Arabidopsis thaliana Columbia ecotype Col-4, seedlings | cry2 phosphorylation rate, cry2 dephosphorylation rate | −20% −15% −10% −20% −20% −10% | <50 nT >> >> >> >> >> | 30 60 90 30 60 90 min | 3 >> >> >> >> >> | Student’s t-test | Magnetometer, 3-axis, spatial distribution, GMF: ~45 μT | Helmholtz coils (axis) | Ø 88 cm | 0.6 (Q2) | [102] |

16 | Arabidopsis thaliana, seedlings, wild type or cry1cry2 mutants, phyAB mutants | Seed germination: Wt Blue light: 50, 60, 70 h Darkness: 50 h cry1cry2 mutants Blue light: 50, 60, 70 h, darkness Hypocotyl length Wt Blue light Darkness cry1cry2 mutants Blue light Darkness phyAB mutants Blue light, Darkness | −50% −60% −45% −50% −80% −50% −40% N/A N/A −50% −30% −40% −40% N/A | <200 nT >> >> >> >> >> >> >> >> >> >> >> >> >> | 96 h >> >> >> >> >> >> >> >> >> >> >> >> >> | 50 >> >> >> >> >> >> >> >> >> >> >> >> >> | Student’s t-test | Magnetometer, 1-axis, spatial distribution, GMF: ~50 μT | μ-Metal chamber and Helmholtz coils (1-axis) | 25 cm × 40 cm Ø 18 cm | 0.68 (Q1) | [103] |

#### 3.3. Effects of HMC on Cell Level

_{2}O

_{2}production, in the fibrosarcoma HT1080 and pancreatic cancer AsPC-1 cell lines [112] and protect the leukemic cell lines HL-60, HL-60R, and Raji from apoptosis, caused by heating [113]. However, in other work, HMC (5 days, 500 nT) caused an increase in lipid peroxidation [114,115]. Notably, mutations in the retinoid receptor (HL-60R lineage) did not affect the effects of HMC [113]. The effects of the HMC on cell division in a culture may depend on the concentration of FBS (fetal bovine serum) in the culture medium; the higher the serum concentration, the higher the effect of the magnetic field [108]. One of the mechanisms for triggering signaling cascades in cells by HMC is a decrease in the concentration of Ca

^{2+}in the cytoplasm of cells [109].

#### 3.4. Effects of HMC at the Molecular Level In Vivo

_{2}O

_{2}production) [39]. HMC led to a decrease in O

_{2}consumption by cells, but the expression of respiratory chain proteins blw (the catalytic subunit F1 ATP synthase) and cytochrome c1 did not change [51]. There is also evidence of a decrease in the ATP/ADP ratio and mitochondrial potential under hypomagnetic conditions. At the same time, an increase in glucose consumption and lactate concentration and an increase in lactate dehydrogenase activity occur in the cells [50]. With HMC, the rate of human tubulin assembly in vitro decreases almost two-fold. It is noteworthy that after the addition of tau protein, tubulin assembly is almost completely inhibited [35]. Actin assembly in neuroblastoma cells is also inhibited in the HMC [47]. Deterioration of actin assembly contributes to a decrease in migration and adhesion of neuroblastoma cells, and changes in morphology [47]. Nitrogen transport in the body also changes under the influence of HMC: a decrease in the activities of blood aspartate and alanine transferases is observed [81]. Interestingly, hypomagnetic conditions may have a radioprotector effect. Using normal human fibroblasts, it was shown that HMCs reduce the number of DNA fragmentations both in the control and after irradiation with 0.5 Gy of γ-radiation [117]. HMCs also affect chromatin condensation in human cells. HMCs contribute to the accumulation of heavy metals Fe, Mn, Co, Ni, Cr, and Cu in the cells (muscles, brain, etc.) [29,67].

№ | Biological Object | Characteristics | Effect, % | Magnetic Flux Density | Time | N | Statistic | Validation | Experimental Setup | Size or Volume | SJR | Ref. |
---|---|---|---|---|---|---|---|---|---|---|---|---|

1 | Mice (M. musculus) C57BL/6 J adults, 8–10 weeks | Proportions of hippocampal neuron types: BrdU+ cells BrdU+ Grap+ SOD2+ type1 cells BrdU+ Grap+ SOD2+ type1 cells Expression of negative regulation of proliferation genes Expression of oxidative stress response genes | −12% −12% −25% +10 ^{2}–10^{5} times−10 ^{2}–10^{5} times−8% | 170 nT >> >> >> >> >> | 8 weeks >> >> >> >> >> | 10 >> >> >> >> >> | One-way or two-way ANOVA or Student’s t-test | Magnetometer, 3-axis, spatial distribution, ambient magnetic fields, noise, and light were measured. SMF in incubator: 39.4 ± 3.6 μT. AMF: 50 Hz Bt PSD1/2 2.37 nT/√Hz | Helmholtz coils (3-axis) | Ø 50 cm | 5.12 (Q1) | [60] |

2 | Mice M. musculus line C57BL/6 J newborns | Proportions of hippocampal neuron types: BrdU+ cells BrdU+ GFAP+ S100β- cells BrdU+ Ki67+ DCX- cells BrdU+ Ki67+ DCX- cells BrdU+ DCX+ NeuN+ cells BrdU+ DCX- NeuN+ cells Dendrite length | −15–25 −50% −60–99% −60–80% −5–30% −40–50% −5% | 0.17 μT >> >> >> >> >> >> | 4 weeks >> >> >> >> >> >> | 6 >> >> >> >> >> >> | One-way or two-way ANOVA or Student’s t-test | Magnetometer, 3-axis, spatial distribution, ambient magnetic fields, noise, and light were measured. SMF in incubator: 39.4 ± 3.6 μT. AMF: 50 Hz Bt PSD1/2 2.37 nT/√Hz | Helmholtz coils (3-axis) | Ø 50 cm | 5.12 (Q1) | [60] |

3 | Mice, Mus musculus line C57BL/6 neonatal, young (P15), adult (2 months) | Primary brain culture from a region of the brain, hippocampus: Cell diameter, proliferation rate The expression of proteins Nestin, Sox2, Neurod1, GFAP, βIII-tubuline | +50% +30% −50% | <85 nT >> >> | 7 days >> >> | 24 >> | One-way ANOVA and χ^{2} test | Magnetometer, spatial distribution Local MF for cells (incubator): 15.1 ± 2.2 μT GMF for animals: 49.88 ± 1.82 μT | Magnetic shielding chamber and Helmholtz coils (3-axis) | Ø 40 cm | 3.37 (Q1) | [30] |

4 | Human neuroblastoma cell line SH-SY5Y | H_{2}O_{2} productionSuperoxide dismutase activity Cell cycle phase ratio: proportion of S phase in the cell cycle | −50% −60% +200% | <500 nT >> >> | 16 h >> >> | 3 >> >> | Shapiro–Wilk test, one-way ANOVA, Bonferroni post hoc test | Magnetometer 3-axis 3D map GMF: ~45 μT | Permalloy chamber | 10 cm × 10 cm × 10 cm | 3.37 (Q1) | [39] |

5 | Human neuroblastoma cell line SH-SY5Y | Expression of genes regulating survival, cell division, adhesion, apoptosis, functions (a total of 2464 analyzed) | +216 genes −2248 genes | <200 nT >> | 1–4 days >> | 6 >> | One-way ANOVA | Magnetometer, 3-axis, spatial distribution, AFM (control): 50 Hz, 575.7 ± 29.1 nT AFM (experiment): 50 Hz, <12.0 nT | Permalloy chamber | 0.24 m^{3} | 1.45 (Q1) | [49] |

6 | Ansell’s mole-rats (F. anselli), adult | Number of c-Fos-IR+ cells Subcortical nuclei, cortical regions, hippocampus, striatum, and primary motor and primary somatosensory cortices | −50% −40% +60% | ~300 nT >> >> | 1 h >> >> | 22 >> >> | One-way ANOVA, Tukey post hoc test | Magnetometer, 3-axis, spatial distribution, HMF variation: <1% GMF: ~46 μT | Helmholtz coils (1-axis) and μ-metal chamber | Ø 170 cm 2 m × 2 m × 2 m | 1.2 (Q1) | [78] |

7 | Mice, C57BL/6J, 7 weeks old | ROS levels in hippocampus: DG region, CA region Gene expressions: NADPH oxidase 4, eosinophil peroxidase, keratin 1, nitric oxide synthase 2, glutathione peroxidase 3, heat shock protein 1A | +30% +30% +155% +85% +86% +60% −70% −64% | 31.9 nT >> >> >> >> >> >> >> >> | 8 weeks >> >> >> >> >> >> >> >> | 4 >> >> >> >> >> >> >> >> | Double-blind study, unpaired Student’s t-test | Magnetometer 3-axis 1 point, time distribution, HMF variation: < 4.5 nT GMF: ~55 μT Temperature, illumination, and relative humidity equal in all conditions | Helmholtz coils (3-axis) | 2 m × 2 m × 2 m | 1.15 (Q1) | [61] |

8 | Drosophila melanogaster sperm | Cell mobility Oxygen consumption by cells (pmolO _{2}/_{mL}/min/test)Protein expressions: blw (the catalytic subunit F1 ATP synthase), c1 cytochrome, cyt c1 oxidase | −30% −25% N/A | <1 nT >> >> | 6 h >> >> | 200 >> >> | One-way ANOVA, Student’s t-test | Magnetometer, 1-axis, 1 point, GMF: 48 μT | Helmholtz coils | - | 1.15 (Q1) | [51] |

9 | Black Garden Ant (Lasius niger) | Gene expression: MagR cry Protein content: SOD GSR H _{2}O_{2} contentEndogenous amine concentrations: tyramine (TA), octopamine (OA), L-DOPA, dopamine (DA), serotonin (Ser), melatonin (Mel) | +20% −18% +38% −20% −60% −20% −80% −80% −75% −80% +10% | ~40 nT >> >> >> >> >> >> >> >> >> >> | 14 days >> >> >> >> >> >> >> >> >> >> | 30 >> >> >> >> >> >> >> >> >> >> | Kolmogorov–Smirnov test, one-way ANOVA, Tukey’s post hoc test | Magnetometer, 3-axis, spatial distribution, HMF variation: < 6 µT GMF: ~42 µT GMF variation: < 20 nT | Helmholtz coils (3-axis) | Ø 128 cm | 1.15 (Q1) | [66] |

10 | Tardigrades (Paramacrobiotus experimentalis) females and males of different age | Mitochondrial potential | −6% | <250 nT | 15 days | 45 | Two-way ANOVA, Tukey post hoc test | Magnetometer 1-axis 1 point GMF: ~50 μT | μ-Metal shielding chamber (approximately 77% nickel, 16% iron, 5% copper, and 2% molybdenum) | 18.5 cm × 12 cm × 33 cm | 1.03 (Q1) | [76] |

11 | Human neuroblastoma SH-SY5Y | Migration and adhesion (rate, distance, cell count) Morphology (outgrowth width) Actin assembly in vitro | −40% - −50% −10% | <200 nT >> <500 nT | 4 days >> 48 h | 4 >> 6 | One-way ANOVA, Chi-square test, Kolmogorov–Smirnov test | Magnetometer, 3-axis, spatial distribution AMF: 12.0 ± 0.0 nT at 50 Hz (in permalloy chamber) SMF: 15.1 ± 2.2 μT; AMF: 575.7 ± 29.1 nT at 50 Hz (incubator) SMF: 52.5 ± 0.4 μT; AMF: 14.0 ± 1.0 nT at 50 Hz (control animals) | Permalloy chamber Helmholtz coils (3-axis) | 50 cm × 50 cm × 50 cm Ø 40 cm | 0.97 (Q1) | [47] |

12 | Mouse embryonic stem cells (mESCs) differentiate into neuronal cells | Expression of neuronal differentiation markers: Huj1 Map2 Proportion of differentiated cells Brachyury expression | −90% −75% −80% −80% | <10 nT >> >> >> | 12 days >> >> >> | 3 >> >> >> | Shapiro–Wilk test, one-way ANOVA, Bonferroni post hoc test, Student’s t-test (normal distribution) | Magnetometer, 3-axis, 1 point | Helmholtz coils (3-axis) | - | 0.97 (Q1) | [107] |

13 | Oriental armyworm; Mythimna separata eggs, larvae, pupae, and imago (females and males) | Vitellogenin Vg gene expression | −50% | <500 nT | 12 h | 300 | One-way or two-way ANOVA | Magnetometer, 1-axis, 1 point, time distribution, HMF variation: < 500 nT | Helmholtz coils | Ø 50 mm | 0.94 (Q1) | [73] |

14 | Human neuroblastoma cell line SH-SY5Y | Number of cells in a culture Proliferation rate Number of cells in G0 phase Number of cells in G1 phase Number of cells in G2/M phase | +8% +8% +7% −7% −5% | <150 nT >> >> >> >> | 2 days >> >> >> >> | 3 >> >> >> >> | One-way ANOVA | Magnetometer, 3-axis, spatial distribution, temperature and relative humidity equal in all conditions, GMF (incubator): < 11 μT GMF (laboratory): ~56 μT | Permalloy chamber | 0.24 m^{3} | 0.89 (Q1) | [108] |

15 | Fibrosarcoma HT1080 and pancreatic AsPC-1 cancer cells | H_{2}O_{2} production | −12% | 500 nT | 24 h | 3 | One-way ANOVA | Magnetometer, 3-axis, spatial distribution, HMF variation: 0.5–2 µT Temperature variation: < 0.1 °C GMF: ~45 μT | μ-Metal cylinder and Helmholtz coils (3-axis) | Ø 12.5 cm | 0.89 (Q1) | [112] |

16 | Cow (Bos taurus) and human (Homo sapiens) | Self-assembly rate of tubulin from α/β-subunits: no tau protein in the presence of tau (recombinant human tau23) protein | −40% −90% | 10–100 nT >> | 20 min >> | 7 >> | Tsou’s method | Magnetometer 1-axis 1 point GMF: ~50 μT | Helmholtz coils (1-axis) | Ø 40 cm | 0.79 (Q1) | [35] |

17 | Human neuroblastoma cell line SH- SY5Y | Proliferation rate Glucose consumption Lactic acid concentration Lactate dehydrogenase activity ATP concentration ADP/ATP ratio Mitochondrial potential | +12% +22% +18% +7% +13% −9% −10% | <200 nT; >> >> >> >> >> >> | 72 h >> >> >> >> >> >> | 3 >> >> >> >> >> >> | Two-way ANOVA, Tukey’s post hoc test (multiple comparisons, Student’s two-tailed t-test (two groups) | Magnetometer, 3-axis, spatial distribution, AMF: 50 Hz, <12.0 nT SMF (control incubator) 15.1 ± 2.2 μT; AMF: 50 Hz (control incubator), 575.7 ± 29.1 nT | Permalloy chamber | 50 cm × 50 cm × 50 cm | 0.79 (Q1) | [50] |

18 | Brown planthopper, S. furcifera males and females, imago | Gene expression cry1 cry2 Adipokinetic hormone concentration Expression Adipokinetic hormone receptor | −20% +10% +10% −17% +25% | ~477 nT >> >> >> >> | 1–5 days >> >> >> >> >> | 40 >> >> >> >> >> | One-way or two-way ANOVA | Magnetometer, 1-axis, spatial distribution (0–1.06 μT) GMF: ~50 μT | Helmholtz coils (3-axis) | Ø 30 cm | 0.74 (Q1) | [45] |

19 | Human bronchial epithelial cell line BEAS-2B after X-ray exposition (1 Gy/min) | Survival, DNA fragmentation, γH2AX expression, Colocalization coefficient of γH2AX and p53BP1 | +6% 0% −40% +40% | 50 nT. >> >> >> | 30–320 min >> >> >> | 3 >> >> >> | One-way ANOVA | Magnetometer, 1-axis, spatial distribution, SMF (incubator): 6–13 μT GMF: ~47 μT | Permalloy chamber Helmholtz coils (3-axis) | Ø 40 cm | 0.43 (Q3) | [118] |

20 | Human fibrosarcoma cell line HT1080 and human colorectal cancer cell line HCT116 | Proliferation | −19% | 200 nT | 1–3 days | 9 | One-way ANOVA | Magnetometer, 1-axis, spatial distribution, SMF (incubator): 6–13 μT GMF: ~43 μT | Helmholtz coils (3-axis) | Ø 50 cm | 0.43 (Q3) | [104] |

21 | Jurkat cells | Anti-CD3-antibody-induced Ca^{2+} influx characteristics:Basal slope: G0/G1 phase cells, S phase cells Reak: G0/G1 phase cells, G2-M phase cells Active intercept: G0/G1 phase cells, S phase cells, G2-M phase cells Active average: G0/G1 phase cells, G2-M phase cells | +20% −10% +4% −12% +104% +83% +81% +82% +65% | <300 nT >> >> >> >> >> >> >> >> | 20 min >> >> >> >> >> >> >> >> | 10 >> >> >> >> >> >> >> >> | MANOVA or paired Student’s t-test | Magnetometer, 1-axis, 1 point AMF variation: <1 nT | μ-Metal chamber | 33 cm × 38 cm × 20 cm | 0.43 (Q3) | [119] |

22 | Human umbilical vein endothelial cells (HUVECs) | Proliferation eNOS expression VEGF gene expression | N/A N/A N/A | 300–500 nT | 24 h | 3 | Student’s t-test | Magnetometer, 3-axis, spatial distribution, SMF (incubator): 6–12 μT | Helmholtz coils and μ-metal chamber | 8.5 cm × 12.5 cm × 6.5 cm | 0.43 (Q3) | [34] |

23 | Mice M. musculus line C57BL/6 newborns (E18) | Viability of femoral muscle myocytes Proportion of cells in apoptosis and necrosis Myosin packaging quality Residual glucose, mM Glycogen, μmool/g protein ATP, μmool/g protein ADP/ATP ratio | −5–10 N/A qualitatively +10% +10% −60 +60–80 | <1 μT >> >> >> >> >> >> | 3 days >> >> >> >> >> >> | 11 6 12 >> | One-way ANOVA or Student’s t-test | Magnetometer, 3-axis, 3D map SMF (control incubator): 38–55 μT AMF: 55–62 Hz, 105. ± 19.2 nT | Helmholtz coils (3-axis) | Ø 40 cm | 0.42 (Q3) | [86] |

24 | Human adults, healthy blood cells | Activity of aspartate aminotransferase Activity of alanine aminotransferase Hemolysis | −12% −28% +9.5 times | 100 nT >> >> | 72 h >> >> | 10 >> >> | Student’s t-test | Magnetometer, 1-axis, 1 point GMF: ~50 μT | Helmholtz coils | - | 0.4 (Q3) | [81] |

25 | Mice M. musculus line CD-1 adults 24–26 g, males | fMLF or PMA induces ROS production by peritoneal granulocytes | −25% | 20 nT | 1.5 h | 10 | Student’s t-test | Magnetometer, 1-axis, spatial distribution Ambient GMF: ~42 μT AMF: 50 Hz, 15-50 nT | Permalloy chamber | - | 0.18 (Q4) | [82] |

26 | Rat (Rattus norvegicus) newborns | Cytosolic Ca^{2+} concentration | −8% | ~300 nT | 7 days | 3 | Student’s t-test | Magnetometer, 1-axis, 1 point GMF: ~48 μT | Nanomaterial-based ASM AMAG 172 chamber | - | 0.18 (Q4) | [109] |

27 | Mice M. musculus C57BL/6 (4–6 weeks old), male | Condition of skeletal muscle cells Citric acid concentration in muscles Number of SS mitochondria Mitochondrial length | qualitatively −30% −20% +15% | 1.12 μT >> >> >> | 30 days >> >> >> | 10 >> >> >> | Kolmogorov–Smirnov test, one-way ANOVA, Student’s t-test, or Mann–Whitney U-test | Magnetometer 3-axis 3D map SMF variation: < 430 nT AMF: 120 Hz, <230 nT | Helmholtz coil (3-axis) | Ø 40 cm | 0.13 (Q4) | [85] |

28 | Rat, Rattus norvegicus line Wistar | Proportion of c-fos+ neurons in the thalamus Proportion of active MOROP3+ neurons in the thalamus and periaqueductal area Proportion of active MOROP3+ neurons in the frontal cortex and superior colliculus | −20% −80% −2% | 50–150 nT >> >> | 21 days >> >> | 12 >> >> | Wilcoxon signed-rank test, Kolmogorov–Smirnov test | Magnetometer, 3-axis, 1 point, HMF variation: < 50 nT | Helmholtz coils | Ø 50 cm | - | [58] |

29 | Brown planthopper Nilaparvata lugens adults, macropterous and brachyppterous | Stability of expression of AK and α-Tub1 | −75% | 523 nT | 2000 h | One-way ANOVA, benchmarks of Cohen for small effects | Magnetometer, 3-axis, one point, HMF variation: < 2% GMF: 50 μT | Helmholtz coils | Ø 120 cm | 1.03 (Q1) | [116] | |

30 | Murine osteoblastic cell line MC3T3-E1 | Cell proliferation, Cell area Cell cycle phase duration: S, G2/M, Fe concentration in medium, Ca concentration, Nodule area, Total protein Gene expression: ALP, BSP, CoI, DMP1, OC, TfR1 | N/A +20% −20% +20% −10% −20% −60% +10% +20% −15% +40% −30% +80% +80% | 500 nT >> >> >> >> >> >> >> >> >> >> >> >> >> | 48 h >> 24 h >> 8 days 8 days >> >> 8 days >> >> >> >> >> | 3 >> >> >> >> >> >> >> >> >> >> >> >> >> | One-way ANOVA, Newman–Keuls test | Magnetometer, spatial distribution, AMF in control incubator 50 Hz ~1 μT AMF in an experimental incubator 50 Hz, < 12 nT GMF: ~45 μT | Permalloy chamber | 550 × 420 × 420 m | 0.73 (Q1) | [110] |

#### 3.5. Effects of HMC on Bacteria

#### 3.6. Effects of HMC on Solutions

№ | Biological Object | Characteristics | Effect, % | Magnetic Flux Density | Time | N | Statistic | Validation | Experimental Setup | Size or Volume | SJR | Ref. |
---|---|---|---|---|---|---|---|---|---|---|---|---|

1 | Pseudomonas (strain P3) Enterobacter (strain E1) | MIC for antibiotics: ampicillin, kanamy, tetracycline, ofloxacin, ceftazidime, tetracycline, ofloxacin | +80% −90% +30% −30% −50% −80% −60% | <500 nT >> >> >> >> >> >> >> | 6 days >> >> >> >> >> >> >> | 6 >> >> >> >> >> >> >> | Student’s t-test | Magnetometer, 1-axis, 1 point | Helmholtz coils | - | 0.55 (Q2) | [122] |

2 | Magnetospirillum magneticum | Magnetosome size Gene expression: mms13, mms6, magA | −9% +70% −10% N/A | <500 nT >> >> >> | 16 h >> >> >> | >300 >> >> >> | Two-way ANOVA, two-tailed Student’s t-test, Mann–Whitney U-test | Magnetometer, 3-axis, spatial distribution, stability HMF area: 200 mm × 200 mm × 200 mm | Helmholtz coil | Ø 1050 mm | 0.53 (Q2) | [32] |

3 | E. coli | MIC for antibiotic (proportions of analyzed strains): ofloxacin, kanamycin, tetracycline, ceftazidime, ampicillin | −9% +12% −19% +12% −10% | ~40 nT >> >> >> >> | 6 days >> >> >> >> | 6 >> >> >> >> | Two-tailed Student’s t-test | Magnetometer, 1-axis, 1 point | Helmholtz coils | Ø 40 cm | 0.4 (Q3) | [121] |

4 | Escherichia coli strain K12 AB1157 in stationary growth phase | Maximum relative viscosity | −18% +18% | 30, 60, or 80 nT 45, 70, or 95 nT | 15 min >> | 15 >> | Student’s t-test | Magnetometer, 3-axis, spatial distribution, AFM: 50 Hz, <30 nT | Helmholtz coils (2-axis) | Ø 19.6 cm | 0.43 (Q3) | [140] |

## 4. Potential Effects of HMC on Organisms Depending on Induction

## 5. Mechanisms of Action of Hypomagnetic Conditions on Living Systems

^{–9}eV, which is seven orders of magnitude less than kT at physiological temperatures. Energy values in hypomagnetic conditions are even lower. Thus, the energy approach to explain magnetobiological effects of this kind is meaningless [150].

#### 5.1. Probable Mechanisms of Static Magnetic Field Effects

- (1)
- action of the Lorentz force on charged particles;
- (2)
- participation of stable magnetic nanoparticles;
- (3)
- radical pair mechanism;
- (4)
- level mixing mechanism.

#### 5.1.1. The Action of the Lorentz Force on Charged Particles

#### 5.1.2. Nanoparticles with Magnetic Properties

#### 5.1.3. Radical Pair Mechanism

^{T}→ A• + B•

^{S}→ A• + B•

_{2}O

_{2}generation due to the formation of singlet oxygen during the S-T transition has been experimentally shown [181,182].

^{–9}s, rarely 10

^{–7}s. This lifetime is the thermal relaxation time of the electron spins (unless the chemical process occurs too quickly). The relaxation time must be large enough for the magnetic field to noticeably change the state of the spins relative to each other. However, this is practically impossible to implement in biological systems at a temperature of ~300 K [156]. However, for permanent HMCs, this is not critical. The minimum magnetic field induction at which magnetic effects begin to occur can be calculated using the formula 1/γτ, where τ is the thermal relaxation time of the moment, and γ is the gyromagnetic ratio, or the ratio of the magnetic dipole moment of a particle to its angular momentum (depends on target) [164]. For electrons in enzyme–substrate complexes, τ = 10

^{–9}s; in this case, the induction value is 5 mT, which is 100 times greater than the geomagnetic field. For an induction of at least 5 μT, often observed with nonspecific effects, the relaxation time must exceed 1 μs. It is still unclear whether conditions are possible in living tissue that ensure such a long relaxation with the participation of electrons [183]; however, in the case of a radical pair, a similar process is possible [184]. However, in bacteria and plants, the effects of magnetic fields have been found to depend on the reversal of the magnetic field and the frequency of the alternating magnetic field, and specific mechanisms such as radical pairs do not exhibit these properties [155]. The RPM is insensitive to magnetic field reversals because, in this case, the magnetic field changes the dynamics of a pair of magnetic moments relative to each other [67].

#### 5.1.4. Level Mixing Mechanism

#### 5.2. Specific Responses

^{+}) [150].

_{2}•

^{−}) [201,202]. Flavin semiquinone, superoxide, and radical scavenger are considered to be a single radical triad system that plays a crucial role in the magnetosensitivity of a cryptochrome [201].

^{3}photons/s (cloudy moonlit night), and 10

^{5}photons/s (clear weather) [206,207]. According to calculations, a value of 1 photon/s is too low to implement the magnetoreception mechanism with the participation of radical pairs, but a value of the order of >10

^{3}photons/s may be sufficient [150]. Interestingly, birds prefer to migrate in clear weather, above or below clouds [208], indicating a requirement of a luminous flux of at least 10

^{3}photons/s per photoreceptor. Consequently, the mechanism of radical pairs can theoretically be implemented during magnetoreception. There are suggestions about additional localization of cryptochromes in the retinal ganglia, but no ordered structures of “candidates” for the role of magnetoreceptors have been found [209,210].

^{+}and gains an unpaired electron. Thus, a pair of radicals with opposite charges (NAD

^{•−}, tryptophan

^{•+}) and antiparallel spins (singlet state) is formed. An external magnetic field can cause a radical pair to transition to the triplet state (parallel spins). In the state of parallel spins, NAD can attach the missing H

^{+}, which is accompanied by conformational rearrangements of cryptochromes, triggering signaling cascades with the further release of signaling molecules, in the case of birds, and neurotransmitters [150].

_{3}O

_{4}) and/or maghemite (γ-Fe

_{2}O

_{3}). Such nanoparticles have been found in many organisms from bacteria [214] to humans [215]. Different types of magnetotactic bacteria use nanoparticles to orientate themselves in space [216,217]. For this purpose, nanoparticles are assembled inside special organelles named magnetosomes [218]. In addition, magnetosomes are used to store excess metals in bacteria. Metals storage is considered a primary function of magnetosomes [219]. About several dozen special genes (mam and mms) participate in the formation of magnetosomes and about 300 more enhance transcription in the process of magnetosome formation in the cell [220].

^{6}iron atoms. If we assume that these 40 atoms possess a solitary magnetic moment, their energy in a magnetic field would be five orders of magnitude lower than the energy of kT.

## 6. Dependence of Biological Effect Magnitude on Quantitative Characteristics of HMC

^{3}s), a day (8.64 × 10

^{5}s), and a month (~2.6 × 10

^{6}s). Therefore, for a further analysis, we used only data on magnetic field induction during HMC.

## 7. Conclusions

## Author Contributions

## Funding

## Institutional Review Board Statement

## Informed Consent Statement

## Data Availability Statement

## Conflicts of Interest

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**Figure 1.**Dynamics of global publishing activity by keywords: magnetic field + biology, magnetic field + cell biology, magnetic field + biochemistry (according to https://pubmed.ncbi.nlm.nih.gov/, accessed on 2 October 2023).

**Figure 2.**The value of magnetic field induction when modeling HMC (references in Table 1). Each point is the value of magnetic field induction indicated in the literature. The color indicates the method for simulating HMC: orange—compensation using Helmholtz coils, blue—shielding using soft magnetic materials. The induction ranges of the magnetic fields of the Earth and objects in space closest to the Earth are shown using shaded areas. *—p < 0.05, Mann–Whitney Rank Sum Test. A total number of analyzed experimental points is 350. The results are shown as medians (box centers) with percentiles 25% and 50% (box bottom and top) and percentiles 10% and 90% (bars).

**Figure 3.**Main directions of effects of HMC on animals. The arrows indicate the direction of the effect: decrease (down) or increase (up) of the parameter. The center shows examples of the most commonly studied model organisms: humans, rodents, insects, and aquatic animals (references in Table 1).

**Figure 4.**The main directions of the effects of hypomagnetic conditions on the morphology and physiology of plants. Arrows indicate the direction of the effect: decrease (down) or increase (up) in the parameter (references in Table 1).

**Figure 5.**Main directions of effects of hypomagnetic conditions at the molecular–cellular level. Arrows indicate the direction of the effect: decrease (down) or increase (up) of the parameter (references in Table 1).

**Figure 6.**Proven or most probable mechanisms of action of magnetic fields on living systems of different levels, and their biological effects (references to the literature and explanations are in the text). Symbols "?" indicate currently unknown targets. Pink colour indicates non-specific effects of HMC. Orange colour indicates specific responses. Blue colour indicates mechanisms of action of magnetic fields on living organisms.

**Figure 7.**The distribution of biological effect values is dependent on methodology (

**a**) and journal rating (

**b**). Metrology in this case included HMC homogeneity analysis: measure of magnetic flux in one time and spatial point without variation description (

**left**) or measure of magnetic flux in serial time and spatial points with variation description (

**right**). Journal rating was based on SJR and actual quartiles (taken from https://www.scimagojr.com/journalrank.php, accessed on 25 October 2023). Each point is an experimental value from an analyzed article. The effects were calculated as the ratio of the difference between the values of the investigated parameter in HMC and Sham control and the value in Sham control. The result was expressed as a percentage. Percentage values were taken modulo. The total number of analyzed experimental points is 350. The results are shown as medians (box

**centers**) with percentiles 25% and 50% (box

**bottom**and

**top**) and percentiles 10% and 90% (bars).

**Figure 8.**Distribution of mean values of biological effects by induction (B) and duration. The effect is calculated as the ratio of the difference between the values of the investigated parameter in GMU and Sham control and the value in Sham control. The result was expressed as a percentage. Percentage values were taken modulo.

**Figure 9.**The distribution of HMC biological effects at the cell level depends on the object of study: cells (

**left**) and organisms (organisms). The effects were calculated as the ratio of the difference between the values of the investigated parameter in HMC and Sham control and the value in Sham control. Absolute values of relative effects in papers are presented as the “Effect, %”. The total number of analyzed experimental points is 350. “*”—p-level < 0.05. Mann–Whitney rank sum test was used.

**Figure 10.**The distribution of HMC biological effects at the cell level depends on the object of study. (

**a**) Box plots of the general distribution of the biological effect between different groups. The results are shown as medians (box

**centers**) with percentiles 25% and 50% (box

**bottom**and

**top**) and percentiles 10% and 90% (bars), (

**b**) dot plots of distribution of biological effect in different groups depending on magnetic field induction. Colors show different objects: cyan—gene expression change; green—protein concentration and enzyme activity; yellow—concentrations of metabolites and other biologically active compounds, and mitochondria functions; magenta—cell survival, proliferation rate, and distribution between cell circle phases; red—cell morphology, differentiation marker surface expression, migration, adhesion, specific electrical responses, etc. The effects were calculated as the ratio of the difference between the values of the investigated parameter in HMC and Sham control and the value in Sham control. Absolute values of relative effects in papers are presented as the “Effect, %”. Total number of analyzed experimental points is 350.

**Figure 11.**The distribution of HMC biological effects at the organism level depends on the object of study. (

**a**) Box plots of the general distribution of the biological effect between different groups. The results are shown as medians (box

**centers**) with percentiles 25% and 50% (box

**bottom**and

**top**) and percentiles 10% and 90% (bars), (

**b**) dot plots of the distribution of biological effects in different groups depending on magnetic field induction. Colors show different objects: cyan—quantity and quality of offspring, speed of growth and development, size of adults; blue—structure and function of muscles and bones; green—concentrations of metabolites, microelements, hormones, and other biologically active compounds (measured in whole organ or organism); yellow—brain’s structure and behavior test results; red—heartbeat rate, microcirculation rate; magenta—survival, regeneration, etc. The effects were calculated as the ratio of the difference between the values of the investigated parameter in HMC and Sham control and the value in Sham control. Absolute values of relative effects in papers are presented as the “Effect, %”. The total number of analyzed experimental points is 350. “*”—p-level < 0.05. Kruskal–Wallis one-way ANOVA on ranks and Dunnett’s post hoc test were used.

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## Share and Cite

**MDPI and ACS Style**

Sarimov, R.M.; Serov, D.A.; Gudkov, S.V.
Hypomagnetic Conditions and Their Biological Action (Review). *Biology* **2023**, *12*, 1513.
https://doi.org/10.3390/biology12121513

**AMA Style**

Sarimov RM, Serov DA, Gudkov SV.
Hypomagnetic Conditions and Their Biological Action (Review). *Biology*. 2023; 12(12):1513.
https://doi.org/10.3390/biology12121513

**Chicago/Turabian Style**

Sarimov, Ruslan M., Dmitriy A. Serov, and Sergey V. Gudkov.
2023. "Hypomagnetic Conditions and Their Biological Action (Review)" *Biology* 12, no. 12: 1513.
https://doi.org/10.3390/biology12121513