Human interaction with ionizing radiation has
evolved from passive environmental exposure to a complex interface
defined by advanced medical diagnostics, nuclear industry expansion
and long-duration space exploration (1). While acute radiation syndrome (ARS)
resulting from high-dose exposure is characterized, the biological
consequences of chronic, low-dose-rate (LDR) exposure represent a
knowledge gap (2). It is
necessary to distinguish CRI from the delayed effects of acute
radiation exposure (DEARE). While DEARE refers to late-onset
pathology emerging months to years following an acute
high-dose/high-dose-rate exposure, CRI results from protracted LDR
irradiation over months to years, characterized by continuous
sublethal damage accumulation, cell senescence and inflammaging
(3).
Unlike the rapid cell ablation seen in acute
scenarios, CRI is characterized by persistent, progressive
pathological changes (4). LDR
exposure triggers a unique interplay of mitochondrial dysfunction
and cytosolic DNA sensing pathways (cyclic GMP-AMP-STING
(cGAS/STING), leading to a Senescence-Associated Secretory
Phenotype (SASP, a complex pro-inflammatory secretome produced by
senescent cells) (5). This
inflammaging microenvironment drives progressive fibrosis, immune
dysregulation and genomic instability distinct from acute injury
patterns (6). Consequently, the
linear no-threshold model-which assumes that biological risk is
directly proportional to radiation dose without any safe lower
limit-often fails to predict the non-linear, stochastic risks of
chronic exposure, necessitating re-evaluation through dedicated
experimental systems (7).
Animal models of CRI are key tools for deconvoluting
these complex biological responses (8). They provide the only rigorous means
to isolate the effects of dose rate from total absorbed dose,
enabling the study of temporal damage accumulation vs. repair
kinetics (9). Moreover, these
models serve as the platforms for the rigorous validation of
next-generation medical countermeasures (MCMs) targeting late-onset
effects of both CRI and acute high-dose irradiation (DEARE), such
as radiation-induced lung fibrosis and secondary malignancy
(10). However, the fidelity of
current CRI models faces scrutiny (11). Many historical models using
fractionated acute irradiation inadequately mimic the continuous,
low-intensity stress of environmental LDR (12-14). Furthermore, translating findings
from inbred rodent strains to genetically diverse human populations
is challenging due to species-specific differences in telomere
biology and immune surveillance (13). Future models must integrate
humanized systems and reflect the heterogeneity of real-world
exposure (14).
Complementing experimental data with epidemiological
evidence from human cohorts provides a foundational understanding
of the long-term risks associated with chronic radiation. Long-term
follow-up studies of Chernobyl liquidators and Fukushima cleanup
workers have revealed elevated risks of non-cancerous pathologies,
such as cataracts and circulatory disease, alongside increased
incidences of leukemia and thyroid cancer (15-17). Similarly, occupational cohorts of
nuclear power plant workers and healthcare professionals,
particularly interventional radiologists and cardiologists,
demonstrate an association between cumulative low-dose exposure and
hematopoietic dysregulation or genomic instability (16,17). However, human studies are
typically confounded by lifestyle variables, inaccurate
retrospective dosimetry and the substantial latency period between
exposure and symptomatic manifestation. These limitations highlight
the translational gap that necessitates the development of
high-fidelity animal models (17). By accurately simulating human
exposure paradigms under controlled conditions, these models enable
the identification of insidious molecular mechanisms such as niche
remodeling and SASP-driven inflammaging that remain elusive in
retrospective human analyses. Thus, integrating human
epidemiological findings with mechanistic animal studies is key for
establishing evidence-based occupational safety thresholds and
precision radioprotection strategies (18).
The present review provides a comprehensive critique
of the methodological and conceptual evolution of CRI animal
models. The present study collected literature across major
databases, including PubMed (pubmed.ncbi.nlm.nih.gov/), Scopus (scopus.com/), and Web of Science (webofscience. com/)
from inception up to December 2025, specifically focusing on LDR
irradiation, mechanistic modeling (SASP, oxidative stress) and
translational countermeasures. The present study aimed to summarize
advances in continuous external exposure and internal radionuclide
contamination models, highlighting their relevance to modern
radiobiology. The present study aimed to address the identification
of robust cross-species biomarkers, including circulating microRNAs
(miRs) and inflammatory signatures, as well as the integration of
single-cell multi-omics into model validation, proposing a
forward-looking framework to enhance the translational power of
chronic radiation research (Fig.
1).
Populations at risk extend beyond traditional
nuclear industry workers to include interventional radiologists,
astronauts exposed to galactic cosmic rays and residents in high
background radiation areas (23). Unlike the rapid onset of acute
symptoms, CRI is characterized by a latent window, in which
sub-clinical metabolic reprogramming and oxidative fluctuations
occur prior to symptomatic manifestation (24). This progression complicates early
risk stratification, rendering traditional biodosimetry markers
ineffective and posing a challenge for precision radiation
protection (Table I) (25).
CRI is a systemic disease, propagated by complex
inter-organ signaling rather than isolated tissue injury. The
hematopoietic system serves as the most sensitive biological
indicator and primary responsive target of LDR toxicity (26). Beyond direct DNA damage to
hematopoietic stem cells (HSCs), chronic exposure remodels the bone
marrow microenvironment (27).
Radiation-induced stromal senescence and adipogenesis (fatty
marrow) create a hostile niche that fails to support HSC
self-renewal, leading to HSC exhaustion, persistent cytopenia and a
pre-leukemic state of clonal instability (28). The immune system undergoes a
paradoxical shift termed inflammaging. While radiation depletes
naïve lymphocyte pools (immunosenescence), damage-associated
molecular patterns released from stressed cells trigger the
cGAS/STING pathway, driving a sustained release of pro-inflammatory
cytokines (IL-6, TNF-α) (29).
This chronic low-grade inflammation not only impairs pathogen
clearance but also creates a tumor-permissive microenvironment
(30). The central nervous
system (CNS), previously considered radioresistant, exhibits
vulnerability through neuroinflammation and the inhibition of
hippocampal neurogenesis, manifesting as cognitive rigidity
(diminished mental flexibility and impaired adaptation to changing
environmental demands) and autonomic dysregulation (31). Furthermore, reproductive toxicity
involves germline DNA fragmentation and endocrine axis disruption,
creating a cycle of systemic physiological decline amplified by
oxidative stress (32).
The molecular hallmark of CRI is genomic
instability, a state where the genome acquires an increased
tendency to alteration. Unlike the transient reactive oxygen
species (ROS) burst in acute exposure, CRI establishes a cycle of
chronic oxidative stress driven by mitochondrial dysfunction
(33). Leakage of electrons from
damaged electron transport chains generates persistent ROS, causing
continuous oxidative base damage-specifically the formation of
8-oxo-7,8-dihydro-2'-deoxyguanosine (34). Damage is not confined to directly
irradiated cells (35). Through
the radiation-induced bystander effect, irradiated cells transmit
distress signals (via exosomes and gap junctions) to non-irradiated
neighbors, propagating genomic instability (36). Studies highlight the role of
epigenetic drift (aberrant DNA methylation and histone
modifications) in locking cells into a dysfunctional state
(37,38). These heritable epigenetic marks
explain why radiation effects persist after exposure ceases,
potentially affecting unexposed offspring via transgenerational
inheritance (Fig. 2) (38).
A key long-term consequence of CRI is the elevation
of stochastic carcinogenic risk (39). According to the LNT model,
chronic accumulation of DNA mis-repairs increases the probability
of malignant transformation (40).
Under continuous immune pressure and oxidative
stress, somatic cells with advantageous mutations (in TP53 or DNA
methyltransferase 3A) may undergo clonal expansion, a phenomenon
known as clonal hematopoiesis of indeterminate potential (41). This clonal evolution serves as a
precursor to radiation-induced leukemias and solid tumors (42).
Compared with spontaneous cancer,
radiation-associated malignancies exhibit distinct mutational
signatures and extended latency periods (43). The spectrum includes leukemia,
thyroid papillary carcinoma and lung fibrosis-associated cancers
(44). These mechanistic
insights underscore the need for refined radiobiological models
that recapitulate these stochastic events to guide international
occupational safety standards (Fig.
3; Table II).
The translational validity of animal models hinges
on the fidelity with which they replicate the physics and dosimetry
of human exposure (45). While
acute high-dose models are well-established, simulating the
protracted nature of CRI requires precise control over dose
accumulation, temporal distribution and linear energy transfer
(LET) (46-48). Existing methodological approaches
use X-ray and γ-ray sources (60Co, 137Cs) due
to their stable energy output and tissue penetration profiles
(47,48). However, the field is evolving
from static exposures to sophisticated dynamic systems that
decouple DR from total absorbed dose, enabling the differentiation
between repairable sublethal damage and cumulative irreversible
injury (48).
External beam irradiation is the cornerstone of
radiobiological modeling, categorized by the extent of anatomical
coverage. Whole-body irradiation (WBI) is the standard for
simulating systemic catastrophe, such as large-scale nuclear
accidents or prolonged occupational exposure in unshielded
environments (49). By
delivering a homogeneous dose across all physiological
compartments, WBI effectively reproduces the syndromic nature of
RI, capturing the interplay between bone marrow failure
(hematopoietic syndrome) and systemic immune collapse (50). A challenge in WBI is achieving
dosimetric homogeneity (51).
Variations in animal geometry can lead to hot spots (overdose) or
cold spots (underdose), potentially confounding survival data
(52). Furthermore, WBI
typically induces lethal acute GI toxicity before chronic fibrotic
phenotypes manifest (53). To
address this, fractionated low-dose regimens are employed to allow
animals to survive the acute phase and develop late-onset pathology
(54). To mimic scenarios such
as localized radiotherapy toxicity or partial shielding, partial
body irradiation selectively targets specific organs (thorax,
brain) while sparing the bone marrow (55). Research has moved beyond lead
shielding to use small animal radiation research platforms
(56). These systems employ
micro-CT guidance to deliver conformal radiation beams with
sub-millimeter precision (57).
This allows the study of organ-specific radiosensitivity
(radiation-induced lung fibrosis) without the confounding variable
of systemic hematopoietic collapse (Fig. 4) (58).
Emerging evidence suggests CRI is not solely the
result of direct energy deposition but is also mediated by NTEs
(59). Models of indirect
irradiation focus on how radiation signals are propagated through
the microenvironment (60-63). Bystander and abscopal models
investigate how irradiated cells communicate with non-irradiated
neighbors via gap junctions, exosomes and soluble factors (ROS,
cytokines) (61). By irradiating
a specific volume (such as the liver) and assessing damage in
distant organs (such as the lung), researchers can elucidate the
systemic propagation of inflammatory signals (62). In ecological toxicology contexts,
indirect exposure also refers to the interaction with irradiated
media (water or soil) (63).
These models are essential for distinguishing between direct
radiotoxicity and the secondary toxicity of radiation-induced
chemical species (radiolysis products) (64).
While external beams simulate prompt exposure,
internal contamination is the most biologically faithful model for
occupational hazards (such as uranium mining) or post-accident
fallout (65). The pathology is
dictated by the chemical nature of the radionuclide (66). For example, osteotropic isotopes
(90Sr, 226Ra) accumulate in the bone matrix,
causing chronic marrow suppression and osteosarcoma, whereas
radioiodine (131I) targets the thyroid (67). These models require precise
calculation of body burden (the total amount of a radionuclide
present in the organism at a given time) and effective half-life
(68). Internal models are key
for studying high-LET radiation (α-particles from plutonium or
radon) (69). Unlike low-LET
γ-rays, α-particles cause dense ionization tracks and complex DNA
double-strand breaks that are refractory to repair (70). This biological insult highlights
the limitation of using external X-rays to mimic internal α-emitter
contamination (71).
To bridge the gap between laboratory conditions and
real-world catastrophes, advanced models integrate multiple
stressors (72,73). Real-world exposure typically
co-occurs with trauma or burns (73-75). Specialized facilities-such as
gamma gardens (open-field irradiation facilities equipped with a
central radioactive source) or prolonged housing near radioactive
sources (60Co or 137Cs)-allow continuous
exposure over months (0.05-0.50 Gy/week) (75). These models are suited to test
the dose-rate effect (the phenomenon where the biological
effectiveness of a radiation dose decreases as the rate of delivery
is reduced, primarily due to ongoing cellular repair), providing
key data for setting occupational safety thresholds and validating
environmental risk models (Table
III) (76).
Animal models of CRI are defined by a distinct
phenotypic landscape that diverges from acute syndromes (77). These models capture the
progressive, multidimensional failure of organ systems driven by
the continuous accumulation of sublethal damage and the propagation
of SASP (77,78).
Chronic radiation accelerates immunosenescence,
characterized by thymic involution and a functional paralysis of
the adaptive immune repertoire (86). Peripheral T cell pools become
oligoclonal, dominated by exhausted memory phenotypes
(PD-1+) with decreased proliferative capacity (87). Simultaneously, the innate immune
system enters a state of hyper-activation known as inflammaging
(88). Irradiated macrophages
activate the NLRP3 inflammasome and the cGAS/STING pathway,
secreting a constant stream of pro-inflammatory cytokines (IL-1β,
IL-6) (89). This immune
dysregulation creates a permissive microenvironment that impairs
pathogen clearance and reduces immunosurveillance against
neoplastic transformation (90).
Physiologically, these changes translate into
sickness behaviors, such as lethargy, anxiety-like thigmotaxis and
cognitive rigidity (95).
Furthermore, radiation disrupts the hypothalamic-pituitary-adrenal
axis, leading to circadian dysregulation (96). This neuro-immune-endocrine
crosstalk highlights the systemic nature of CRI, where CNS injury
exacerbates peripheral immune suppression (Fig. 5) (97).
The utility of any animal model is determined by the
balance between its face (phenotypic similarity to humans) and
construct validity (mechanistic similarity). Compared with
fractionated acute doses, LDR sources more accurately replicate the
continuous radiation exposure patterns associated with occupational
hazards and environmental contamination (98). LDR models capture the abscopal
interactions between organs (such as the kidney-heart axis),
allowing for the evaluation of holistic therapeutics rather than
single-organ protectants (99).
The latency of CRI requires extended housing (6-24 months),
increasing costs (100). The
confounding factor of aging becomes critical; distinguishing
radiation effects from natural geriatric decline requires robust
age-matched controls (101).
Rodents possess different metabolic rates and DNA repair kinetics
than humans (102). For
example, the lethal dose required to kill 50% of the population
within 30 days) varies, complicating the direct extrapolation of
dose-response associations (103).
Selecting the appropriate model involves ensuring a
match between the specific biological mechanisms under
investigation and the inherent physiological attributes of the
chosen animal (104).
The utility of a preclinical model relies on its
construct validity, the fidelity with which it recapitulates the
human pathological landscape (120). Establishing a standardized
validation framework is key, as CRI presents a subtle, non-linear
progression distinct from the clear endpoints of acute syndrome
(121). A robust validation
strategy must triangulate data across physiological performance,
hematological integrity, histopathological architecture and
molecular signatures, providing systems-level corroboration of
radiation toxicity (122).
Physiological metrics serve as the frontline
indicators of systemic stress and sickness behavior, typically
preceding clinically detectable organ failure (123). Unlike the rapid weight loss
seen in acute syndrome, chronic radiation induces a wasting
phenotype akin to cancer cachexia (124). Longitudinal monitoring
typically reveals a blunted growth trajectory or gradual BMI
decline, driven by hypothalamic inflammation and sustained
catabolic signaling (125).
Clinical frailty index, an aggregate score of deficits (alopecia,
gait anomalies, grip strength), is a superior metric for
quantifying radiation-induced accelerated aging compared with body
weight alone (126). Changes in
feeding behavior reflect the disruption of the gut-brain axis
(127). Radiation-induced
mucositis and hypothalamic dysregulation manifest as anorexia and
polydipsia (128). A sustained
20-30% decline in caloric intake suggests a transition from
transient stress to chronic metabolic dysregulation (129). Quantitative behavioral assays
are key for validating CNS injury (130). Automated tracking using open
field test and Morris water maze detects decreased locomotor
velocity (lethargy), anxiety-like thigmotaxis and cognitive
deficits in spatial memory (131). These behavioral phenotypes are
associated with hippocampal neuroinflammation and serve as
non-invasive biomarkers for successful model induction (132).
Peripheral blood analysis provides a dynamic liquid
biopsy of the bone marrow microenvironment (133). In CRI models, the validation
endpoint is lineage skewing (a persistent imbalance in the
production of different hematopoietic cell types that reflects
underlying marrow dysfunction and stem cell injury. While acute
exposure causes rapid pancytopenia, chronic exposure typically
leads to a myeloid-biased output (increased granulocyte/lymphocyte
ratio) at the expense of lymphopoiesis, a hallmark of hematopoietic
aging (134). Progressive,
refractory normocytic anemia (hemoglobin <100 g/l) and elevated
red cell distribution width serve as diagnostic criteria for
cumulative marrow failure (135). Flow cytometric profiling must
assess functional status (136). Validated models demonstrate an
inverted CD4/CD8 ratio and the expansion of regulatory T cells
(137,138). Upregulation of exhaustion
markers on T cells-specifically programmed cell death protein 1
(PD-1) and T-cell immunoglobulin and mucin domain-containing
protein 3, along with decreased natural killer cell cytotoxicity,
provide definitive immunophenotypic evidence of chronic radiation
stress (138).
Histopathology remains the gold standard for
defining irreversible tissue remodeling (139). However, modern validation
requires specific staining and digital quantification beyond
standard hematoxylin and eosin staining (140). A pathognomonic feature of CRI
is the replacement of hematopoietic cellularity with adipose tissue
(141). Validated models
demonstrate a quantifiable shift in the marrow
adipocyte-to-hematopoietic cell ratio (142-144). A hallmark of late-stage CRI is
the excessive deposition of extracellular matrix (143). Validation should utilize
Masson's trichrome or Sirius Red staining to visualize collagen
(144). Immunohistochemistry
for α-smooth muscle actin (identifying myofibroblasts) is key for
distinguishing active fibrogenesis from static scarring (145). To enhance reproducibility,
studies employ AI-driven image analysis algorithms to score
fibrosis area fraction and cellularity, eliminating inter-observer
variability inherent in manual scoring (145,146).
A model is considered validated only when it
satisfies this multidimensional matrix: Exhibiting the phenotypic
frailty, hematological skewing, histological fibrosis and the
molecular SASP signature characteristic of human CRI pathology
(Fig. 7; Table V) (155).
Animal models of chronic radiation injury allow the
mapping of complex signal transduction networks that drive chronic
pathology (158,159). Chronic LDR exposure triggers a
senescence-like arrest distinct from acute apoptosis (159). Models have been pivotal in
identifying the p53-p21 axis as the gatekeeper of this arrest and
the subsequent activation of NF-κB, which drives the SASP (160,161). This demonstrates how irradiated
cells survive but remain metabolically active, propagating
inflammation to bystander tissue (161). epigenetic scars (persistent,
long-term alterations in the epigenome (such as stable changes in
DNA methylation patterns) that continue to drive abnormal gene
expression long after the initial radiation exposure has ceased
(162,163). High-throughput bisulfite
sequencing in chronically exposed rodents has identified persistent
hypermethylation of tumor suppressor promoters
(p16INK4a) and global hypomethylation of
retrotransposons (163).
Integrative multi-omics (transcriptomics + metabolomics) has mapped
the dysregulation of the tricarboxylic acid cycle and fatty acid
oxidation, providing a systems-level view of radiation-induced
metabolic rewiring (164).
The primary industrial application of animal models
of chronic radiation injury is the rigorous screening of MCMs,
distinguishing between prophylactic agents (pre-exposure) and
mitigators (post-exposure) (165). In the screening phase, models
quantify the dose reduction factor of candidate agents (166). Effective agents must
demonstrate significant preservation of the HSC pool and a
reduction in marrow adiposity (167). Research has moved beyond free
radical scavengers to targeted therapy (168). Models are validating senolytics
(navitoclax, quercetin) that selectively eliminate senescent cells
to rejuvenate tissue (168,169). Furthermore, pharmacodynamic
studies optimize dosing to mitigate DEARE, ensuring that agents do
not interfere with DNA repair in a manner that promotes secondary
carcinogenesis (Table VII)
(57,170).
Beyond pharmaceuticals, models are key for testing
holistic strategies suitable for long-term occupational exposure
(171). Comparative studies
demonstrate that dietary polyphenols and probiotics remodel the gut
microbiome, which is often dysbiotic after radiation (171,172). This gut-bone marrow axis
modulation enhances Nrf2-ARE signaling, the master regulator of
antioxidant defense, thereby decreasing systemic oxidative stress
(malondialdehyde levels) (173). Controlled exercise studies
reveal that mechanical loading upregulates AMPK signaling,
promoting mitochondrial biogenesis (174,175). This counteracts
radiation-induced sarcopenia and fatigue, offering a
non-pharmacological strategy for astronauts or nuclear workers
(175).
Animal models provide the empirical data necessary
to construct AOPs, which link a molecular initiating event (such as
DNA oxidation) to an adverse outcome (such as fibrosis). By
exposing large cohorts to low-dose rates, researchers test the
validity of the LNT model vs. hormesis (adaptive response)
(176,177). This data is critical for
setting occupational limits (such as for interventional
cardiologists) (178).
Real-world risk involves combined stressors (179). Advanced models simulate the
exposome by co-exposing animals to radiation in the presence of
heavy metals (such as uranium mining) or microgravity (spaceflight)
(178,179). These studies reveal synergistic
toxicities that single-stressor models miss, refining ecological
risk assessments (179,180).
Future mechanistic inquiry will transcend bulk
tissue analysis to identify the spatiotemporal dynamics of injury
(189). By integrating
single-cell RNA sequencing with spatial transcriptomics,
researchers may move beyond merely identifying which cells are
damaged to understanding where they are located relative to the
niche (190). This will map the
neighborhood effects (how a senescent stromal cell spatially
corrupts adjacent stem cells via SASP) (191). Advanced genetic fate-mapping
will unveil the clonal trajectories of surviving cells,
distinguishing between regenerative and pre-leukemic clones
(192). This high-resolution
mapping may identify specific molecular switch points (such as
epigenetic loci) that determine whether a tissue undergoes repair
or irreversible fibrosis (193).
The therapeutic landscape is shifting from symptom
management to disease modification (194). A notable frontier is the
targeting of senescent cells (195). Future models will rigorously
validate senolytics (drugs that induce apoptosis in senescent
cells) and senomorphics (agents that suppress SASP without killing
the cell) (196). The goal is
to restore the irradiated microenvironment to a pre-exposure state
(197). While SC therapy holds
promise, the future may lie in extracellular vesicles (EVs) and
exosomes (198). Derived from
mesenchymal SCs, these cell-free cargoes carry regenerative miRs
and proteins with lower immunogenicity and tumorigenic risk than
live cells (199). Models
optimize engineered EVs loaded with specific radioprotective cargos
(mitochondria or mRNA) for targeted delivery (199,200). Clustered regularly interspaced
short palindromic repeats-associated protein 9 and base editing
in vivo will evolve toward correcting radiation-induced
mutations in somatic tissue or epigenetically silencing
pro-fibrotic genes (TGF-β) via modifiable promotors (201).
While the present review provides a methodological
framework for CRI modeling, limitations must be acknowledged.
First, due to the logistical, ethical and financial constraints of
conducting life-span studies in large animal models (such as
non-human primates), the majority of the mechanistic data,
particularly regarding SASP and inflammaging, is derived from
murine models. Extrapolating these rodent-derived mechanisms to
humans requires extreme caution, given the species-specific
differences in telomere dynamics, metabolic rate and immune
surveillance. Second, experimental models traditionally isolate
radiation as a single stressor to maintain controlled variables.
However, real-world human exposure (spaceflight or nuclear
accidents) typically involves complex exposome interactions, such
as concomitant exposure to heavy metals, psychological stress or
microgravity, which may alter the CRI trajectory. Finally, spatial
multi-omics and AI-driven digital twins are currently in their
early developmental or conceptual phases and require empirical
validation before widespread translational application.
In conclusion, CR animal models are transitioning
from descriptive pathology to predictive precision medicine
(211). This may facilitate
development of robust, personalized defenses against adverse health
effects of ionizing radiation (212).
Not applicable.
ZX, XiaodongL, ChunhuiY, LW, JM, QLiu, CL, QLi, YH,
JW, ChengzhuoY, FS, ChaoY, MW, BY, YL, QH, LZ, XuemeiL and
XiaobingL wrote the manuscript and constructed figures. XuemeiL and
XiaobingL edited the manuscript and supervised the study. Data
authentication is not applicable. All authors have read and
approved the final manuscript.
Not applicable.
Not applicable.
The authors declare that they have no competing
interests.
The authors would like to thank Professor Sheng Li
(Chongqing Medical and Pharmaceutical College, Chongqing, China)
for providing expert guidance on the conceptual framework and
feedback during the preparation of the manuscript.
The present study was supported by 2023 Chongqing Medical
Scientific Research Project (Joint Project of Chongqing Health
Commission and Science and Technology Bureau; grant no.
2023GGXM006), Joint Project of Chongqing Health Commission and
Science and Technology Bureau (Joint Key Laboratory Open Project)
(grant no. 2026KFXM051), Natural Science Foundation of Chongqing
(grant no. CSTB2025NSCO-GPX1116), 2026 Chongqing Municipal Health
Commission Traditional Chinese Medicine Research Project (grant no.
2026WSJK158), Technological Innovation Project of Shapingba
District, Chongqing (grant no. 2025016), 2024 Scientific research
Project of Chongqing Medical and Pharmaceutical College (grant no.
ygzrc2024101), Chongqing Municipal Education Commission Youth
Project (grant nos. KJQN202302811, KJQN202502819 and
KJQN202402821), 2024 Chongqing Medical and Pharmaceutical College
Innovation Research Group Project (grant no. ygz2024401), Science
and Health Joint Medical Research Project of Shapingba District,
Chongqing (grant no. 2024SQKWLHMS051), 2025 Teaching Research &
Reform Project of Chongqing Medical and Pharmaceutical College
(grant no. YGZJG2025322), The Key Laboratory Project of Chongqing
Medical and Pharmaceutical College (grant no. YGZPT2025101), 2025
Scientific Research Project of Chongqing Medical and Pharmaceutical
College (grant no. YGZZK2025116), 2025 Technological Innovation
Project of Shapingba District, Chongqing (grant no. 2025031) and
Joint project of Chongqing Health Commission and Science and
Technology Bureau (grant no. 2024MSXM115).
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