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DOI 10.11603/ijmmr.2413-6077.2022.1.12903

STRUCTURAL ORGANIZATION OF RAT TISSUES IN EXPERIMENTAL 
COMBINED TRAUMA OF THE CHEST AND BOTH THIGHS

*M. Marushchak¹, O. Mialiuk2, M. Kaskiv2, M. Demjanchuk2, I. Krynytska1
1 – I. HORBACHEVSKY TERNOPIL NATIONAL MEDICAL UNIVERSITY, TERNOPIL, UKRAINE

2 – RIVNE MEDICAL ACADEMY, RIVNE, UKRAINE

Background. In cases of severe trauma, fractures of long bones are the most often combined with trauma 
of the chest, head, and abdomen, as well as development of hemorrhagic shock. Therefore, it is reasonable to 
study the combined trauma of the chest and lower extremities in details, as well as the post-traumatic multiple 
organ dysfunction especially in early manifestation stage. 

Objective. The aim of the study was to identify the features of structural organization of the lungs, heart 
and liver with underlying combined trauma of the chest and both thighs on the 7th day of the post-traumatic 
period.

Methods. The experimental study involved 22 adult nonlinear white male rats with body mass of 200-210 g, 
kept on a standard diet at animal facility with food and drinking regimes recommended by the standards for 
laboratory animals. All animals were divided into 2 groups: the control group (1st, n=10), the experimental group 
(the 2nd) chest trauma and both thighs trauma, observation for 7 days (n=12). The animals of the experimental 
group were simulated for right-sided closed pneumothorax with a rib fracture by a trocar under thiopental-sodium 
anesthesia (40 mg/kg of body weight of the rat, intraperitoneally); it was combined with a fracture of the left and 
right femurs. Skeletal injury was modeled on each thigh that caused a closed fracture by a single dosed blow 
with a specially designed device. The blow energy was 0.375 J that corresponds to a severe injury. The associated 
injury was simulated by successive infliction of both injuries. 

Results. Examination of the liver of animals on the 7th day of the experiment revealed a rapid growth of 
lesions in their parenchyma. The central veins were poorly visible and contained single erythrocytes; the vessels 
of medium caliber of myocardial stroma were dilated and blood-filled, which was manifested by the development 
of perivascular oedema. In the lungs of experimental animals, a moderate decrease of interstitial tissue oedema 
of the interalveolar septa was present, while cellular infiltration of mast cells, macrophages and lymphocytes 
also decreased significantly. 

Conclusions. Multiple organ injuries, which are characterized by structural changes in the liver, heart and 
lungs in the combined trauma of the thorax and thighs on the 7th day of experiment were evidenced.

KEYWORDS: combined trauma; lungs; heart; liver; morphology.

*Corresponding author: Mariya Marushchak, Professor, I. Hor-
bachevsky Ternopil National Medical University, Ternopil, 
46002, Ukraine. 
E-mail: marushchak@tdmu.edu.ua

International Journal of Medicine and Medical Research 
2022, Volume 8, Issue 1, p. 81-87
copyright © 2022, TNMU, All Rights Reserved

M. Marushchak et al.

Introduction 
At the present time, the significant increase 

of multiple and combined traumatic injuries is 
one of the major health problems in Ukraine as 
well as in many countries around the world, [1] 
that leads to polysystemic and multiorgan 
lesions, which in turn increase mortality rate 
[2, 3]. The most common injuries and major 
causes of death are traumatic brain injury [4] 
and chest injury [5]. According to other re-
search, limb fractures predominate in the struc-
ture of polytrauma [6, 7]. In the case of severe 
trauma, fractures of long bones of the extre-

mities are most often combined with trauma 
of the chest, head, and abdominal organs, as 
well as development of hemorrhagic shock [8]. 
It is established that among patients with 
trauma, the frequency of polytrauma is 13.7%, 
and polytrauma with combined multiple frac-
tures of long bones of the lower extremities is 
0.5% [9]. The same authors note that more than 
70% of chest injuries, traumatic brain injuries, 
and injuries of the musculoskeletal system 
(16.7% of patients have fractures of the lower 
extremities) dominate as for the localization. 
Therefore, it is reasonable to study the com-
bined trauma of the chest and lower extremities, 
as well as the post-traumatic multiple organ 
dysfunction especially in early manifestation 
stage (on the 7th day). 



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The aim of the study was to define the 
features of the structural organization of the 
lungs, heart and liver with underlying combined 
trauma of the chest and both thighs on the 7th 
day of the post-traumatic period.

Methods 
The experimental study involved 22 adult 

nonlinear white male rats weighing 200-210 g, 
which were kept on a standard diet of vivarium 
with food and drinking regimes at the level 
recommended by the standards for laboratory 
animals. All animals were divided into 2 groups: 
the control group (1st, 10 animals); the experi-
mental group (2nd) – chest trauma and both 
thighs trauma (CT + 2T), observation during 7 
days (12 animals). The animals of the experi-
mental group were simulated right-sided 
closed pneumothorax with a rib fracture by a 
trocar under thiopental-sodium anesthesia 
(40 mg/kg of the body weight of the rat, intrape-
ritoneally); it was combined with a fracture of 
the left and right femurs. Skeletal injury was 
modelled on each thigh that caused a closed 
fracture by applying a single dosed blow by a 
specially designed device [10]. The blow energy 
was 0.375 J, which corresponds to a severe 
injury. The associated injury was simulated by 
successive infliction of both injuries. While 
working with animals, the rules of handling 
experimental animals were followed. Mortality 
rate of animals was 16.7%.

Samples of heart, liver and lung tissues, 
under the conditions of simulated associated 
trauma and correction, were fixed with 1.5% 
solution of glutaraldehyde in 0.2 M cacodylate 
buffer (pH 7.2) at t=4 °C for 1 h. The samples 
were washed with cacodylate buffer and addi-
tionally fixed with a 2% solution of osmium 
tet ro xide in the same buffer for 1 h (t=4 °C). The 
preparations were washed from the fixatives 
and dehydrated in increasing concentrations 
of ethyl alcohol (50%, 70%, 90% and 100%). 
Additionally, they were dehydrated in 2 changes 
of propylene oxide and placed in epoxy resin 
epon-812. The sections were obtained using an 
ultramicrotome UMTP-6 and a diamond knife, 
they were contrasted with 2% uranyl acetate 
solution for 15 min and additionally with lead 
citrate according to Reynolds. Sections were 
observed and photographed using an electron 
transmission microscope PEM-100.

All animal studies have been approved by 
the appropriate bioethics committee of I. Hor-
bachevsky Ternopil State Medical University 
(protocol № 41 of June 1, 2017).

Results 
In the most severe period of the maximum 

probability of complications (from 3 to 10 days) 
development of respiratory hypoxia, cardio vas-
cular disorders, metabolic acidosis, programmed 
and induced cell death is possible. During this 
period the syndrome of multiple organ dys-
function is diagnosed. Therefore, liver, heart 
and lungs were investigated as target organs 
in multiple organ dysfunction during associated 
trauma in 7 days of the experiment. Examination 
of the liver of animals in 7 days of the experiment 
revealed a rapid growth of lesions in its pa-
renchyma. The central veins were poorly visible 
and contained single erythrocytes. The lumens 
of the sinusoids were practically not visualized, 
but erythrocytes were traced in their single 
preserved areas (Fig. 1). The lobular organization 
of hepatocytes was disturbed, the vast majority 
of cells did not have a clear structure, their 
contours were not clear, the size was difficult 
to visualize. The cytoplasm of hepatocytes of 
all parts of the lobe was devastated, enlightened, 
or granular (Fig. 1), which indicated development 
of severe protein hyaline-droplet and hydropic 
dystrophy with transition to focal necrosis 
(Fig. 1). The vast majority of nuclei was crump-
led, became smaller, or disappeared, but in 
some cells they were visualized with loose 
chromatin, multiple nucleoli. Intercellular con-
nections were largely lost.

Uneven blood supply and focal lympho- and 
histiocytic perivascular infiltration were ob­
served in the vessels of the portal tracts.

In 7 days of the experiment, the vessels of 
medium calibre of myocardial stroma were still 
dilated and blood­filled, which was manifested 
by development of perivascular oedema. Di-
lated capillaries and diapedesis of erythrocytes 
were found in the fibre thickness. Cardio myo­
cytes were well visualized in the vast majority 
of visual fields, but focal intracellular myo-
cytolysis and pyknotically altered nuclei were 
evidenced in some of them, indicating the 
presence of focal dystrophic-necrotic changes. 
The perivasal stroma was loosened due to 
oedema, which also spread to the intercellular 
spaces, disintegrating the muscle layer (Fig. 2).

In 7 days of the experiment in the lungs of 
the experimental animals a moderate decrease 
of interstitial tissue oedema of the interalveolar 
septa was evidenced, while cellular infiltration 
of mast cells, macrophages and lymphocytes 
a l s o  d e c r e a s e d  s i g n i f i c a n t l y .  S i g n s  o f 
dystelectasis (partial decline) were still present 

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that led to a decrease in the airiness of the lung 
t i s s u e .  S o m e  p n e u m o c y t e s  u n d e r w e n t 
dystrophic-necrotic changes, and a small 
amount of exfoliated epithelium and serous 
exudate appeared in the lumens of the alveoli 
(Fig. 3). The blood supply to the vessels was still 
uneven, with a predominance of venous 
capillary ones. Leukocytes focally accumulated 
in the perivascular spaces (Fig. 3).

Discussion 
The severity of the patient’s condition with 

trauma is largely determined by development 
of various metabolic disorders in organs and 
tissues with underlying severe endotoxicosis 
[11]. These pathological phenomena cause 
development of deregulatory pathology, one 
of the manifestations of which is multiorgan 

Fig. 1. Structural changes in the liver in cases of simulation of combined trauma in 7 days of the experiment 
(acute hyaline-drip and hydropic dystrophy with transition to focal necrosis). Hematoxylin and eosin  stai ning. 
×200.

Fig. 2. The structure of cardiomyocytes in the simulation of associated trauma in 7 days of the experiment 
(pericellular oedema combined with erythrodiapedesis, focal dystrophic changes in cardiomyocytes). He-
matoxylin and eosin staining. ×200.

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failure involving lungs, heart and liver into the 
pathological process. 

According to the pathogenesis shortly after 
the injury the systemic inflammatory response 
syndrome is established. A number of studies 
have shown that oxidative stress is crucial in 
activation of inflammation. From a genetic 
point of view, oxidative stress modulates in-
flammation by regulating the activity of certain 
transcription factors, such as nuclear kappa 
factor B (NF-kB), signal transducer and activator 
of transcription 3 signal transducer and 

activator of transcription 3 (STAT 3), hypoxia 
induction factor 1 alpha (HIF-1- alpha), and 
protein-1 activator (AP-1) [12]. Activation of 
peroxidation processes is one of the factors 
destabilizing the membranes. It is established 
that when hydroxyl radicals influence on diene 
conjugates of fatty acids, lipid hydroperoxides 
are formed, which cause conformational dis-
turbances in the cell membranes. The data 
ob tained indicate that the intensity of peroxi-
dation in different tissues of the body depends 
on the type of injury. Analysis of the scientific 

Fig. 3. Structural changes of the lung in cases of simulation of combined trauma in 7 days of the experi-
ment: A (perivascular accumulation of leukocytes), B (uneven vascular blood supply, dystrophic­necrotic 
changes of epitheliocytes, slight effusion in the lumen of the alveoli, dystelectasis, focal perivascular leu-
kocyte infiltration). Hematoxylin and eosin staining. ×200.

А

B

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sources shows that oxidative stress in the 
patients with various injuries develops almost 
immediately after the initial injury moving from 
the macroscopic level to the cellular and mo-
lecular one [13-15]. Currently, scientists have 
proven that the maximum of lipoperoxidation 
coincides with the intensity of the body’s 
response to inflammation [16]. Thus, Kozak DV 
notes that the intensity of lipoperoxidation due 
to hip injury and blood loss is fluctuating with 
a period of development to the 3rd day, a period 
of temporary well-being in 14 days and a re-
increase in 21 days [17]. The results of the study 
of oxidative processes in the case of combined 
trauma of the chest and both thighs show that 
the most intense free-radical processes occur 
in the lungs on the 7th and 14th days of ob-
servation. On the 3rd day of the experiment, the 
production of mitochondrial superoxide anion 
radical increases equally in the tissues of the 
heart and lungs, while in the tissues of the liver 
this rate increases to a maximum within 3-14 
days [18-20]. It has been established that acute 
hyperproduction of reactive oxygen species by 
leukocytes in 1 day of the experiment causes 
disorganization of bioelectrical activity of mito-
chondrial membranes, which is characterized 
by a dynamic increase in the ratio of leukocyte 
cells suspension with reduced transmembrane 
potential and the ratio of leukocytes with signs 
of apoptosis with a maximum in 7 days [21]. 

In cases of extensive metabolic changes in 
the body tissues of rats with simulated com-

bined trauma, structural changes in the liver, 
heart and lungs after 1-3 days of the experiment 
were evidenced. These changes were mani fes-
ted by severe circulatory disorders, erythrostasis 
and development of dystrophic-necrotic chan-
ges, especially in epithelial structures [22]. 
According to our study, these structural chan-
ges progressed in the lungs, heart and liver up 
to the 7th day of observation that is comparable 
to the severity of oxidative stress in the body 
tissues and apoptotic death of leukocytes.

Conclusions 
In cases of combined trauma of the thorax 

and thighs of the experimental animals, struc-
tural changes develop in the liver, heart and 
lungs on the 7th day of observation. These 
changes are characterized by severe hyaline-
drip and hydropic dystrophy with transition to 
focal necrosis of liver tissue, pericellular 
oedema and dystrophic-necrotic changes of 
pneumocytes.

Conflict of interest
Authors declare no conflict of interest.

Author contributions
Mariya Marushchak, Inna Krynytska – con­

ceptualization, methodology, formal analysis, 
writing – original draft, writing – reviewing and 
editing; Mykhailo Demjanchuk, Oksana Mialiuk – 
data curation, investigation, formal analysis; 
Marjana Kaskiv – writing, original draft.

ОСОБЛИВОСТІ СТРУКТУРНОЇ ОРГАНІЗАЦІЇ ТКАНИН ЩУРА  
ЗА УМОВ ПОЄДНАНОЇ ТРАВМИ ГРУДНОЇ КЛІТКИ ТА ОБОХ СТЕГОН

М. Марущак1, о. Мялюк2, М. Каськів2, М. Демянчук2, і. Криницька1
1 – ТЕРНОПІЛЬСЬКИЙ НАЦІОНАЛЬНИЙ МЕДИЧНИЙ УНІВЕРСИТЕТ ІМЕНІ І. Я. ГОРБАЧЕВСЬКОГО  

МОЗ УКРАЇНИ, ТЕРНОПІЛЬ, УКРАЇНА
2 – КОМУНАЛЬНИЙ ЗАКЛАД ВИЩОЇ ОСВІТИ “РІВНЕНСЬКА МЕДИЧНА АКАДЕМІЯ”  

РІВНЕНСЬКОЇ ОБЛАСНОЇ РАДИ, РІВНЕ, УКРАЇНА

Вступ. За умови тяжкої травми переломи довгих кісток кінцівок найчастіше поєднуються з 
травмою грудної клітки, голови, органів черевної порожнини, розвитком геморагічного шоку Тому, 
обґрунтованим є дослідження поєднаної травми грудної клітки та нижніх кінцівок, а також 
поліорганність їх ураження, особливо у фазу маніфестації.

Мета. Виявити морфологічні особливості структурної організації легень, серця і печінки на тлі 
поєднаної травми грудної клітки та обох стегон через 7 діб моделювання травми.

Методи. Експериментальне дослідження виконано на 22 дорослих нелінійних білих щурах-самцях 
масою 200–210 г, яких утримували на стандартному раціоні віварію з підтриманням харчового і 
питного режимів на рівні, рекомендованому нормами утримання лабораторних тварин. Усіх тварин 

M. Marushchak et al.



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було поділено на 2 групи: контрольну (1-а, 10 тварин), дослідну групу: 2-а – травма грудної клітки й 
обох стегон (ТГК+2С), спостереження 7 діб (12 тварин). Тваринам дослідної групи під тіопентал-
натрієвим наркозом (40 мг/кг маси тіла щура внутрішньочеревно) за допомогою троакара моделювали 
правобічний закритий пневмоторакс із переломом ребра та поєднували їх з переломом лівої і правої 
стегнових кісток. Скелетну травму моделювали шляхом нанесення однократного дозованого удару 
спеціально розробленим пристроєм по кожному стегну, який викликав закритий перелом (Kozak, 2011). 
Енергія удару становила 0,375 Дж, що відповідало травмі важкого ступеня тяжкості. Поєднану травму 
моделювали шляхом послідовного нанесення обох ушкоджень. 

Результати. Дослідження печінки тварин через 7 діб експерименту встановило різке зростання 
ураження її паренхіми. Центральні вени проглядалися слабо, міс тили поодинокі еритроцити, судини 
середнього калібру строми міокарда залишалися розширеними та наповненими кров’ю, що проявилося 
розвитком перивакулярного набряку. У легенях піддослідних тварин спостерігалося помірне зменшення 
набряку інтерстиціальної тканини міжальвеолярних перегородок, а також значно зменшилась клітинна 
інфільтрація тучними клітинами, макрофагами та лімфоцитами.

Висновки. При поєднаній травмі грудної клітки та стегон експериментальних тварин структурні 
зміни в печінці, серці та легенях на 7 добу спостереження, що характеризуються вираженою гіаліново-
крапельної та гідропічної дистрофії з переходом у вогнищеві некрози тканин печінки, перицелюлярним 
набряком, поєднаним з еритродіапедезом, вогнищевими дистрофічними змінами кардіоміоцитів та 
дистрофічно-некротичними змінами пневмоцитів.

КЛЮчоВі сЛоВа: поєднана травма; легені; серце; печінка; морфологія.

Information about the authors 
Mariya Marushchak, Professor, I. Horbachevsky Ternopil National Medical University, Ternopil, Ukraine
https://orcid.org/0000­0002­1177­412X, e­mail: marushchak@tdmu.edu.ua
Oksana Mialiuk, Assistant Professor, Rivne Medical Academy, Rivne, Ukraine
https://orcid.org/0000­0002­5090­6607, e­mail: oksankamp@ukr.net
Marjana Kaskiv, Assistant Professor, Rivne Medical Academy, Rivne, Ukraine
https://orcid.org/0000­0002­6914­0867, e­mail: maryana_kaskiv@ukr.net
Mykhailo Demjanchuk, Assistant Professor, Rivne Medical Academy, Rivne, Ukraine
https://orcid.org/0000­0001­8729­5144, e­mail: dmr­rv@ukr.net
Inna Krynytska, Professor, I. Horbachevsky Ternopil National Medical University, Ternopil, Ukraine
https://orcid.org/0000­0002­0398­8937, e­mail: krynytska@tdmu.edu.ua

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6. Probst C, Pape HC, Hildebrand F, Regel G, 
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Almahmoud K, Zhi Q, et al. Characterization of blunt 

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Received 12 May 2022; revised 26 May 2022;  
accepted 7 June 2022.

This is open access article distributed under the Creative Com-
mons Attribution License, which permits unrestricted use, 
distribution, and reproduction in any medium, provided the 
original work is properly cited.

M. Marushchak et al.