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Activated partial thromboplastin time maybe associated with the prognosis of papillary thyroid carcinoma

  • Yanhai Wang , Luying Liu , Pingting Zhou , Xiaoli Luo , Han-Qing Liu EMAIL logo and Hua Yang EMAIL logo
Published/Copyright: October 19, 2022
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Open Chemistry
From the journal Open Chemistry Volume 20 Issue 1

Abstract

Objective

Hemostasis markers associated with tumors have been widely studied. However, the associations between the coagulation factors and papillary thyroid carcinoma (PTC) prognosis remain unclear. The aim of the present study was to investigate these associations.

Patients and methods

PTC patients treated at Shengjing Hospital between 2013 and 2019 were retrospectively analyzed and divided into three groups. Clinical, ultrasound, and pathological patient characteristics were recorded. The blood routine, coagulation factors, and thyroid function data were compared.

Results

A total of 50 patients were selected and divided into Group 1 [complicated with second primary malignancies (SPMs)], Group 2 (with postoperative cervical lymph node metastasis), and Group 3 (control group). The ages of patients in Group 2 were significantly higher than those in the control group. The neutrophil ratio (%) in Group 1 was significantly higher than that in Groups 2 and 3, while its lymphocyte ratio (%) was significantly lower. The coagulation factor activated partial thromboplastin time (APTT) in the first and second groups was statistically significantly lower than that in the control group. There were no statistical differences in APTT between the first and second groups. Shorter APTT was associated with SPM and postoperative cervical lymph node metastasis.

Conclusions

Coagulation indicators, especially APTT, may be a new biomarker for predicting PTC prognosis and may provide a new molecular target, especially in combination with SPM and postoperative cervical lymph node metastasis.

Keywords: papillary thyroid carcinoma; prognosis; coagulation factors; APTT

1 Introduction

Thyroid cancer (TC) is the most prevalent endocrine malignancy and about 80–85% of all cases are papillary thyroid carcinomas (PTCs) [1]. In view of the highly increased prevalence of PTC over the years, it is of great importance to explore its outcomes and influencing factors [2]. While well-differentiated PTC patients generally have good outcomes, the 5-year survival rate in patients with advanced PTC is only 59% [3,4]. In addition, the recurrence of PTC after thyroidectomy is over 5%, which manifest as true soft tissue local recurrence, cervical lymphadenopathy, or distant metastasis [5,6,7]. The increased risk of a second primary malignancy (SPM) in PTC has been reported [8]. SPMs include salivary gland, bone, kidney, ureter, and hematologic malignancies [8]. Identifying the risk factors for PTC recurrence, metastasis, and SPM can help to identify new molecular targets and guide the expansion of surgical scope, early postoperative aggressive chemotherapy and close follow-up [3].

The last decades have delineated many interactions of the hemostatic system with tumor occurrence, progression, metastasis, and recurrence. Different coagulation factors play different roles in TCs [9]. The relationships between coagulation function and TC gained more and more attention. Sagripanti et al. [10] have measured plasma concentration of fibrinopeptide A and D-dimer in 21 thyroidectomized patients and 27 control subjects. They have found that fibrinolysis was enhanced in TC patients with distant metastases and that plasma D-dimer levels are useful biomarkers to monitor this condition. Franchini et al.[11] have analyzed the hemostatic balance in different thyroid disorders using literature reviews and concluded that hyperthyroidism is generally accompanied by hypercoagulable states, whereas the hemostatic profile in hypothyroidism and TC depends on the severity of the disease. Nielsen et al. [12] have reported a case undergoing removal of a malignant thyroid tumor, whose hypercoagulability was mediated by hemeoxygenase-1. Ordookhani et al. [13] have reviewed studies on venous thromboembolism and TC and concluded that further studies are necessary, as the results would influence clinical practice for the necessity of anticoagulants use in some TC groups.

These studies have suggested that clotting factors may be potential biomarkers for TC prognosis. However, the relationship between coagulation dysfunction and PTC prognosis, especially the influence on recurrence, metastasis, and complications with SPM remains unclear. The present study aimed to reveal it.

2 Patients and methods

2.1 Patients

Patients with PTC after surgery who were followed up routinely with ultrasound and computed tomography (CT) were retrospectively analyzed between January 2013 and December 2019. The present study was approved by the Ethical Review Board of Shenzhen Samii Medical Center (Grant no. SSMC-202103-19).

2.2 Inclusion and exclusion patient criteria

Inclusion criteria were as follows: (1) PTC patients confirmed by pathology; (2) patients who had undergone radical surgery of the thyroid for the first surgery and took different doses of thyroxine tablets orally according to the result of thyroid function analysis; (3) no postoperative radiation or chemotherapy was administered; and (4) the follow-up period was ended upon when the ultrasound or CT examination of the patient was suspected abnormal. Patients with diabetes mellitus, hypertension, autoimmune disease, acute or chronic infection, hematologic disease, heart failure, myeloproliferative disorders, hepatic or renal disorders, and bleeding or thrombotic disease were excluded from the study.

2.3 Groups

The patients were divided into three groups according to the different prognoses. Group 1 included patients complicated with SPM. Group 2 consisted of patients with postoperative cervical lymph node metastasis. Group 3 patients served as control group that included those suspected to have postoperative cervical lymph node metastasis or recurrence in the thyroidectomy bed based on the routine ultrasonography examination during the follow-up but were confirmed to be normal by pathology analysis after the second surgery.

2.4 Examining and analyzing the indicators

Epidemiological characteristics of all patients at the first diagnosis with PTC were recorded, including gender, age, blood type, and ultrasound and pathological tumor characteristics. Routine laboratory parameters of all patients before the second surgery were recorded, including data on blood routine examination, thyroid function, and coagulation indicators. All blood samples were obtained in the morning between 7:00 and 8:00 o’clock 3 or 4 days before the second surgery, without any physical exercise after overnight fasting. The same standardized blood tubes were used for sampling. All blood samples were analyzed within 1 h after venipuncture and measured using standard laboratory methods on a biochemistry autoanalyzer (Sysmex XN-9000 automated hematology analyzer, ACLTOP700 automatic coagulation analyzer, and ARCHITECT i2000SR immunoassay analyzer) with the company’s original kits.

The routine blood indicators included white blood cell (WBC) count, neutrophil (NEUT%) ratio, lymphocyte (LYM%) ratio, monocyte (MONO%) ratio, eosinophil (EOS%) ratio, basophil (BASO%) ratio, red blood cell (RBC) count, hemoglobin (HGB) count, and platelet (PLT) count. The thyroid function indicators included triiodothyronine (FT3), thyroxine (FT4), thyroid-stimulating hormone (TSH), thyroid peroxidase antibody (TPOAb), and thyroglobulin antibody (TgAb). The coagulation factors included prothrombin time (PT), prothrombin time activity (PTA), prothrombin international normalized ratio (INR), prothrombin ratio (PTR), activated partial thromboplastin time (APTT), fibrinogen (FIB), thrombin time (TT), and D-dimer.

2.5 Statistical analysis

All analyses were conducted using the SPSS software version 27.0. Continuous variables were expressed as mean ± SD. One-way analysis of variance (ANOVA) was used to compare intergroup differences. Multiple comparisons between groups were compared with LSD. Categorical variables were compared using the Chi-square test (Monte Carlo Sig. T2). A P-value of <0.05 was considered significant.

3 Results

3.1 Epidemiological and clinical characteristics

A total of 5077 PTC patients who underwent surgery and follow-up at the ShengJing Hospital of China Medical University between 2013 and 2019 were retrospectively analyzed. A total of 50 cases were selected to participated in the present study based on the inclusion and exclusion criteria, including 11 in Group 1 (patients complicated with SPM), 16 in Group 2 (patients with postoperative cervical lymph node metastasis), and 23 in Group 3 (control group). The mean intervals of TC and second malignancies were 33 months (7–66 months) and 28 months (11–61 months) in Group 2 with postoperative cervical lymph node metastasis, respectively. For the 11 cases complicated with SPM, there was one case of pancreatic cancer, two of gastric cancer, four of breast cancer, two of lung cancer, one of cervical cancer, and one of intestinal cancer. Figure 1 is a flow diagram of the standards for the patient inclusion and exclusion criteria.

Figure 1 Flow diagram of standards for patient inclusion and exclusion criteria.
Figure 1

Flow diagram of standards for patient inclusion and exclusion criteria.

The epidemiological and clinical characteristics of the three groups are shown in Table 1. Of the 50 cases included, 76% were female, which was consistent with the epidemiological PTC trend. The proportion of women in Group 1 was slightly higher than that in the other groups but showed no statistically significant difference. The ages of patients in Group 2 (54.1 ± 14.7 years) were significantly higher (P < 0.05) than those in Group 3 (43.7 ± 11.8 years). Patients in Group 1 (51.5 ± 10.2 years) was also older than those in Group 3, but there was no statistically significant difference among them. There was one case of peripheral tissue invasion in both Group 1 and Group 2 after the first surgery, but not in Group 3. The rate of lymph node metastasis in Groups 1 and 2 was approximately 1.5 and 2 times that in Group 3, respectively, but there were no significant differences among the three groups. The proportion of tumor calcification was similar in the three groups, but the types were different. In Group 2, the proportion of microcalcification was lower, while the proportion of coarse calcification was significantly higher than that in Group 3 (18.8% vs 0%, P < 0.05). Interestingly, there were obvious differences in blood type composition among the three groups. Patients with type O blood accounted for almost half (45%) of the cohort in Group 1. There were no cases with type AB blood. Patients with type B blood was dominant in Groups 2 (37.5%) and 3 (39.1%). The lowest numbers of patients in Groups 2 and 3 were those of types A (12.5%) and AB (13.0%), respectively. However, whether this difference in blood type has biological significance needs to be investigated in further studies with larger samples. Ultrasound examination revealed that the tumor length in Group 2 was significantly higher than Group 3 (2.1 ± 1.2 cm vs 1.1 ± 0.7 cm, P < 0.01) and tumor of Group 1 (1.7 ± 1.3 cm) was also larger than that in Group 3, but no significant difference was observed.

Table 1

Epidemiological and clinical characteristics of the patients

Groups Total (N = 50) Group 1 (N = 11) Group 2 (N = 16) Group 3 (N = 23)
Gender: female (n, %) 38 (76.0) 9 (81.8) 12 (75.0) 17 (73.9)
Age (years) 48.7 ± 13.2 51.5 ± 10.2 54.1 ± 14.7* 43.7 ± 11.8
Peripheral tissue invasion (n, %) 2 (4.0) 1 (9.1) 1 (6.3) 0 (0)
Lymphatic metastasis after first surgery (n, %) 17 (34.0) 4 (36.4) 8 (50.0) 5 (21.7)
Calcification (n, %) Microcalcification 23 (46.0) 6 (54.5) 6 (37.5) 11 (47.8)
Coarse calcification 3 (6.0) 0 (0) 3 (18.8)* 0 (0)
Mixed calcification 2 (4.0) 0 (0) 0 (0) 2 (8.7)
Without calcification 22 (44.0) 5 (45.5) 7 (43.8) 10 (43.5)
Blood type (n, %) A 10 (20.0) 3 (27.3) 2 (12.5) 5 (21.7)
B 18 (36.0) 3 (27.3) 6 (37.5) 9 (39.1)
O 16 (32.0) 5 (45.5) 5 (31.3) 6 (26.1)
AB 6 (12.0) 0 (0) 3 (18.8) 3 (13.0)
RH+ (n, %) 50 (100.0) 11 (100.0) 16 (100.0) 23 (100.0)
Tumor size (cm) 1.5 ± 1.1 1.7 ± 1.3 2.1 ± 1.2** 1.1 ± 0.7

Group 1: patients complicated with SPM. Group 2: patients with postoperative cervical lymph node metastasis. Group 3: control group. Chi-square test, one-way ANOVA, * P < 0.05, ** P < 0.01, compared with Group 3.

3.2 Blood routine test results

As shown in Table 2, the NEUT (%) in Group 1 was significantly higher than that in Groups 2 and 3 (65.5% vs 56.3% vs 57.4%, P < 0.05), while the LYM (%) in Group 1 was significantly lower than that in Groups 2 and 3 (25.0% vs 34.2% vs 32.1%, P < 0.05). Both NEUT (%) and LYM (%) in Group 2 showed no significant difference compared to Group 3. The PLT in Group 2 was significantly lower than that in Group 1 (199.4 vs 258.2, P < 0.01) and Group 3 (199.4 vs 234.3, P < 0.05). The WBC of Group 2 was lower than that in the other two groups, while its BASO (%) was higher than that in the other two groups and exceeded the upper limit of the normal reference range, although this result was not statistically significant. There were no statistically significant differences among the three groups in items of blood routine parameters, including MONO (%), EOS (%), and RBC and HGB counts.

Table 2

Blood routine test results of the patients

Groups Total (N = 50) Group 1 (N = 11) Group 2 (N = 16) Group 3 (N = 23)
WBC (109/L) 7.2 ± 6.0 7.4 ± 1.9 5.2 ± 1.3 8.4 ± 8.5
NEUT (%) 58.8 ± 10.8 65.5 ± 11.4*,# 56.3 ± 10.1 57.4 ± 10.2
LYM (%) 31.2 ± 9.7 25.0 ± 9.6*,# 34.2 ± 9.7 32.1 ± 8.7
MONO (%) 6.6 ± 2.2 6.4 ± 1.9 6.3 ± 2.2 7.0 ± 2.4
EOS (%) 2.0 ± 1.4 2.0 ± 1.3 1.8 ± 1.3 2.0 ± 1.6
BASO (%) 0.7 ± 1.6 0.3 ± 0.2 1.2 ± 2.7 0.5 ± 0.2
RBC (1012/L) 4.4 ± 0.5 4.3 ± 0.2 4.4 ± 0.5 4.5 ± 0.5
HGB (g/L) 133.2 ± 14.5 131.3 ± 11.3 132.7 ± 16.1 134.5 ± 15.2
PLT (109/L) 228.4 ± 54.0 258.2 ± 71.1## 199.4 ± 40.7* 234.3 ± 44.4

Group 1: patients complicated with SPM. Group 2: patients with postoperative cervical lymph node metastasis. Group 3: control group. One-way ANOVA, * P < 0.05 compared with Group 3. # P < 0.05, ## P < 0.01 compared with Group 2.

Furthermore, the analysis of the proportion of outliers in the above-mentioned blood routine indicators showed that BASO and RBC outliers in Group 1 were significantly higher than those in Groups 2 and 3 (Table 3).

Table 3

Outlier comparison of blood routine test results

Groups Total (N = 50) Group 1 (N = 11) Group 2 (N = 16) Group 3 (N = 23)
WBC (ref: 3.5–9.7 × 109/L) Outlier ratio (n, %) 8 (16.0) 2 (18.2) 2 (12.5) 4 (17.4)
Abnormally high ratio (n, %) 6 (12.0) 2 (18.2) 0 (0) 4 (17.4)
Abnormally low ratio (n, %) 2 (4.0) 0 (0) 2 (12.5) 0 (0)
NEUT (ref: 43.2–71.5%) Outlier ratio (n, %) 9 (18.0) 2 (18.2) 3 (18.8) 4 (17.4)
Abnormally high ratio (n, %) 5 (10.0) 2 (18.2) 1 (6.3) 2 (8.7)
Abnormally low ratio (n, %) 4 (8.0) 0 (0) 2 (12.5) 2 (8.7)
LYM (ref: 16.8–43.4%) Outlier ratio (n, %) 11 (22.0) 2 (18.2) 5 (31.3) 4 (17.4)
Abnormally high ratio (n, %) 6 (12.0) 0 (0) 4 (25.0) 2 (8.7)
Abnormally low ratio %) 5 (10.0) 2 (18.2) 1 (6.3) 2 (8.7)
MONO (ref: 4.6–12.4%) Outlier ratio (n, %) 8 (16.0) 2 (18.2) 3 (18.8) 3 (13.0)
Abnormally high ratio (n, %) 1 (2.0) 0 (0) 0 (0) 1 (4.3)
Abnormally low ratio (n, %) 7 (14.0) 2 (18.2) 3 (18.8) 2 (8.7)
EOS (ref: 0.7–7.8%) Outlier ratio (n, %) 10 (20.0) 2 (18.2) 3 (18.8) 5 (21.7)
Abnormally high ratio (n, %) 0 (0) 0 (0) 0 (0) 0 (0)
Abnormally low ratio (n, %) 10 (20.0) 2 (18.2) 3 (18.8) 5 (21.7)
BASO (ref: 0.2–1.2%) Outlier ratio (n, %) 7 (14.0) 4 (36.4)* 2 (12.5) 1 (4.3)
Abnormally high ratio (n, %) 2 (4.0) 0 (0) 2 (12.5) 0 (0)
Abnormally low ratio (n, %) 5 (10.0) 4 (36.4)*,## 0 (0) 1 (4.3)
RBC (ref: 3.8–5.5 × 1012/L) Outlier ratio (n, %) 5 (10.0) 0 (0) 2 (12.5) 3 (13.0)
Abnormally high ratio (n, %) 1 (2.0) 0 (0) 0 (0) 1 (4.3)
Abnormally low ratio (n, %) 4 (8.0) 0 (0) 2 (12.5) 2 (8.7)
HGB (ref: 115–150 g/L) Outlier ratio (n, %) 8 (16.0) 1 (9.1) 3 (18.8) 4 (17.4)
Abnormally high ratio (n, %) 5 (10.0) 0 (0) 2 (12.5) 3 (13.0)
Abnormally low ratio (n, %) 3 (6.0) 1 (9.1) 1 (6.5) 1 (4.3)
PLT (ref: 135–350/L) Outlier ratio (n, %) 3 (6.0) 1 (9.1) 1 (6.3) 1 (4.3)
Abnormally high ratio (n, %) 2 (4.0) 1 (9.1) 0 (0) 1 (4.3)
Abnormally low ratio (n, %) 1 (2.0) 0 (0) 1 (6.3) 0 (0)

Group 1: patients complicated with SPM. Group 2: patients with postoperative cervical lymph node metastasis. Group 3: control group. Chi-square test, * P < 0.05 compared with Group 3. ## P < 0.01 compared with Group 2.

3.3 Thyroid function test results

The mean levels of FT3, FT4, and TSH in the three groups were all within the normal range and without significant differences, which may be due to the use of drugs to control thyroid levels in all patients experiencing PTC after surgery (Table 4). Interestingly, the mean value of TPOAb in Group 1 was within the normal range, while the mean value of TgAb in Group 1 was close to the normal range. The mean values of the two indexes in Groups 2 and 3 were very high compared to the normal range nearly 10 times higher than the upper limit. However, due to the sizeable variance, there was no significant difference between the three groups.

Table 4

Thyroid function indicators

Groups Total (N = 50) Group 1 (N = 11) Group 2 (N = 16) Group 3 (N = 23)
FT3 (pmol/L) 4.4 ± 0.5 4.4 ± 0.5 4.6 ± 0.6 4.4 ± 0.4
FT4 (pmol/L) 14.9 ± 2.6 14.5 ± 2.1 14.3 ± 2.4 15.6 ± 2.8
TSH (μIU/mL) 2.1 ± 1.6 1.9 ± 1.5 2.8 ± 2.1 1.8 ± 1.3
TPOAb (IU/mL) 28.6 ± 85.4 4.4 ± 13.3 36.4 ± 86.9 34.7 ± 103.2
TgAb (IU/mL) 55.8 ± 168.0 4.4 ± 7.4 113.4 ± 274.1 40.3 ± 87.4

Group 1: patients complicated with SPM. Group 2: patients with postoperative cervical lymph node metastasis. Group 3: control group. One-way ANOVA.

This result was further confirmed by the statistical analysis of each indicator’s outliers. In Groups 2 and 3, a high proportion of patients had an abnormally high TPOAb (25.0% vs 26.1%) and TgAb (37.5% vs 39.1%) (Table 5).

Table 5

Outlier comparison of thyroid function indicators

Groups Total (N = 50) Group 1 (N = 11) Group 2 (N = 16) Group 3 (N = 23)
FT3 (ref: 2.63–5.71 pmol/L) Outlier ratio (n, %) 0 (0) 0 (0) 0 (0) 0 (0)
Abnormally high ratio (n, %) 0 (0) 0 (0) 0 (0) 0 (0)
Abnormally low ratio (n, %) 0 (0) 0 (0) 0 (0) 0 (0)
FT4 (ref: 9.01–19.05 pmol/L) Outlier ratio (n, %) 3 (6.0) 1 (9.1) 1 (6.3) 1 (4.3)
Abnormally high ratio (n, %) 2 (4.0) 1 (9.1) 0 (0) 1 (4.3)
Abnormally low ratio (n, %) 1 (2.0) 0 (0) 1 (6.3) 0 (0)
TSH (ref: 0.3–4.8 μIU/mL) Outlier ratio (n, %) 7 (14.0) 2 (18.2) 2 (12.5) 3 (13.0)
Abnormally high ratio (n, %) 3 (6.0) 1 (9.1) 2 (12.5) 0 (0)
Abnormally low ratio n, %) 4 (8.0) 1 (9.1) 0 (0) 3 (13.0)
TPOAb (ref: 0–5.61 IU/mL) Outlier ratio (n, %) 11 (22.0) 1 (9.1) 4 (25.0) 6 (26.1)
Abnormally high ratio (n, %) 11 (22.0) 1 (9.1) 4 (25.0) 6 (26.1)
Abnormally low ratio (n, %) 0 (0) 0 (0) 0 (0) 0 (0)
TgAb (ref: 0–4.11 IU/mL) Outlier ratio (n, %) 18 (36.0) 3 (27.3) 6 (37.5) 9 (39.1)
Abnormally high ratio (n, %) 18 (36.0) 3 (27.3) 6 (37.5) 9 (39.1)
Abnormally low ratio (n, %) 0 (0) 0 (0) 0 (0) 0 (0)

Group 1: patients complicated with SPM. Group 2: patients with postoperative cervical lymph node metastasis. Group 3: control group. Chi-square test.

3.4 Coagulation function test results

The mean values of PT and TT among the three groups were within the normal range but without significant differences (Table 6). The PTA of the three groups exceeded the normal upper limit, and the level in Group 2 was slightly lower than that in the other two groups. Similarly, the D-dimer level in Group 2 was lower than that in the other two groups, but the difference was not statistically significant. The mean values of all three groups were within the normal range. The INR, PTR and APTT levels in Group 1 were significantly lower than those in Group 3, and its FIB level was significantly higher than that of Group 3. INR and PTR in Group 1 were also lower than those in Group 2. For Group 2, only APTT was significantly lower than that in Group 3.

Table 6

Coagulation factors

Groups Total (N = 50) Group 1 (N = 11) Group 2 (N = 16) Group 3 (N = 23)
PT (s) 10.9 ± 1.6 10.3 ± 0.4 11.2 ± 1.1 11.1 ± 2.2
PTA (%) 110.2 ± 19.9 110.6 ± 16.2 104.5 ± 19.5 113.9 ± 21.6
INR 0.9 ± 0.1 0.9 ± 0.0**,# 1.0 ± 0.1 1.0 ± 0.1
PTR 0.9 ± 0.1 0.9 ± 0.0**,# 0.9 ± 0.1 1.0 ± 0.1
APTT (s) 29.0 ± 5.3 25.9 ± 4.8** 27.1 ± 5.7** 31.9 ± 3.6
FIB (g/L) 2.8 ± 0.7 3.3 ± 0.9* 2.8 ± 0.7 2.7 ± 0.4
TT (s) 18.7 ± 18.7 16.9 ± 1.8 16.3 ± 1.8 21.2 ± 27.6
D-Dimer (μg/L) 179.2 ± 266.9 223.5 ± 437.6 119.1 ± 94.3 199.8 ± 247.9

Group 1: patients complicated with SPM, Group 2: patients with postoperative cervical lymph node metastasis; Group 3: control group. One-way ANOVA, * P < 0.05, ** P < 0.01 compared with Group 3. # P < 0.05 compared with Group 2.

Analysis of the proportion of outliers showed that the proportion of abnormally low PT values in Group 1 was significantly higher than that in the other two groups. The proportion of FIB outliers in Group 1 was significantly higher than that in the other two groups. In addition, the proportion of abnormally high PTA value in Group 1 was twice as high as that in Group 3. The proportion of abnormally high APTT value in Group 2 was twice as high as that in Group 3, but without significant differences (Table 7).

Table 7

Outlier comparison of coagulation factors

Groups Total (N = 50) Group 1 (N = 11) Group 2 (N = 16) Group 3 (N = 23)
PT (ref: 10.5–13.5 s) Outlier ratio (n, %) 14 (28.0) 6 (54.5)* 5 (31.3) 3 (13.0)
Abnormally high ratio (n, %) 0 (0) 0 (0) 0 (0) 0 (0)
Abnormally low ratio (n, %) 14 (28.0) 6 (54.5)* 5 (31.3) 3 (13.0)
PTA (ref: 80–100%) Outlier ratio (n, %) 38 (76.0) 9 (81.8) 11 (68.8) 18 (78.3)
Abnormally high ratio (n, %) 34 (68.0) 9 (81.8) 9 (56.3) 16 (43.5)
Abnormally low ratio (n, %) 4 (8.0) 0 (0) 2 (12.5) 2 (8.7)
INR (ref: 0.8–1.5) Outlier ratio (n, %) 0 (0) 0 (0) 0 (0) 0 (0)
Abnormally high ratio (n, %) 0 (0) 0 (0) 0 (0) 0 (0)
Abnormally low ratio n, %) 0 (0) 0 (0) 0 (0) 0 (0)
PTR (ref: 0.8–1.2) Outlier ratio (n, %) 0 (0) 0 (0) 0 (0) 0 (0)
Abnormally high ratio (n, %) 0 (0) 0 (0) 0 (0) 0 (0)
Abnormally low ratio (n, %) 0 (0) 0 (0) 0 (0) 0 (0)
APTT (ref: 21–37 s) Outlier ratio (n, %) 6 (12.0) 1 (9.1) 3 (18.8) 2 (8.7)
Abnormally high ratio (n, %) 3 (6.0) 0 (0) 1 (6.3) 2 (8.7)
Abnormally low ratio (n, %) 3 (6.0) 1 (9.1) 2 (12.5) 0 (0)
FIB (ref: 2–4 g/L) Outlier ratio (n, %) 7 (14.0) 3 (27.3) 3 (18.8) 1 (4.3)
Abnormally high ratio, n%) 4 (8.0) 3 (27.3)** 1 (6.3) 0 (0)
Abnormally low ratio (n, %) 3 (6.0) 0 (0) 2 (12.5) 1 (4.3)
TT (ref: 13.5–19.5 s) Outlier ratio (n, %) 5 (10.0) 1 (9.1) 2 (12.5) 2 (8.7)
Abnormally high ratio (n, %) 3 (6.0) 1 (9.1) 1 (6.3) 1 (4.3)
Abnormally low ratio (n, %) 2 (4.0) 0 (0) 1 (6.3) 1 (4.3)
D-Dimer (ref: 0–252 μg/L) Outlier ratio (n, %) 8 (16.0) 1 (9.1) 2 (12.5) 5 (21.7)
Abnormally high ratio (n, %) 8 (16.0) 1 (9.1) 2 (12.5) 5 (21.7)
Abnormally low ratio (n, %) 0 (0) 0 (0) 0 (0) 0 (0)

Group 1: patients complicated with SPM, Group 2: patients with postoperative cervical lymph node metastasis; Group 3: control group. Chi-square test, * P < 0.05, ** P < 0.01 compared with Group 3.

4 Discussion

Various hemostasis markers associated with tumor staging and prognosis have been previously studied [14,15]. Elevated D-dimer levels, preoperative plasma prolonged PT level, hyperfibrinogenemia, high D-dimer level, and increased fibrinogen degradation product level may function as hemostasis markers that predict overall survival in gastric cancer patients, operable colorectal cancer patients, and renal, prostate, and bladder cancer patients [14,16,17]. Jianyong et al. [18] have found that PTC cases with preoperative hyperfibrinogenemia are more likely to have an advanced tumor lymph nodes’ metastasis stage and higher rate of PTC recurrence, while serum fibrinogen levels may serve as a biomarker for predicting PTC recurrence, not concerning the other coagulation factors. Uysal et al. [19] have observed that red cell distribution width, mean platelet volumes, hemoglobin content, and plateletcrit were significantly higher in the benign multinodular goiter and PTC groups than in the healthy control group. A possible correlation between APTT and hemoglobin content and tumor size in benign multinodular goiter and PTC was also noted [20,21]. APTT and PT in the PTC group were statistically significantly higher than those in the healthy controls [20]. There is currently no literature focusing on the relationship between the hemostasis markers and different TC prognoses.

The present study evaluated the expression of coagulation factors in samples of PTC with different prognoses to investigate the associations among them. To the best of our knowledge, this is the first study focusing on the biomarkers for the prognosis of PTC with postoperative cervical lymph node metastasis and SPM.

The coagulation system includes endogenous and exogenous coagulation system. PT is a sensitive and commonly used screening test for exogenous coagulation, while APTT is used for the endogenous coagulation system [22]. The shorter PT and APTT may be due to the increased blood viscosity and thromboembolic diseases, while the longer PT and APTT may be due to the opposite condition, such as the lack of some coagulation factors, hyperactivity of anticoagulant and fibrinolytic system, and use of some anticoagulant drugs [23,24]. In the present study, the shortened APTT in PTC patients was associated with SPM and postoperative cervical lymph node metastasis. This indicates that the coagulation factors are related to the different PTC prognoses.

There are few studies focusing on the relationship between APTT and cancer. APTT is increased in renal cancer, but not in prostate and bladder cancers [16]. It has no prognostic value for the survival of patients with hepatocellular carcinoma [25]. APTT in healthy persons is longer compared to non-small-cell lung cancer patients [26]. A possible correlation has been observed among APTT, hemoglobin content, and tumor size in benign multinodular goiter and PTC groups. There is no current literature on the relationship between APTT and multiple cancers. The present study showed that shorter APTT is related to SPM and postoperative cervical lymph node metastasis in PTC patients.

In general, cancer is associated with an imbalance in the hemostatic system and induces a prothrombotic state. However, the molecular and laboratory features of cancer-associated thrombosis are complex and multifactorial and are difficult to assess clinically [26,27]. Several mechanisms may explain the observed impact of the hypercoagulability state. First, several procoagulant molecules, among which tumor necrosis factor is the most important, are expressed by cancer cells or are induced by them in normal vascular tissues via the release of soluble mediators and direct cancer cell host cell contact [28]. Second, the role of various components of the plasminogen activating system, especially urokinase-plasminogen activator and plasminogen activator inhibitor type 1, in TC progression, metastasis, prognosis, and progression-free survival has been established [28,29,30]. Finally, it is unknown to what extent TSH-suppressive thyroid hormone therapy may contribute to the hypercoagulability state in TC patients. Reports on the influence of thyroid hormones on hemostasis, while suggesting a hypercoagulable state in thyrotoxicosis, have often been inconclusive [31].

Although the present study described the APTT levels in TC patients with different prognoses, especially in patients with multiple TCs, the current investigation had some limitations. The cohort consisted of a small number of patients in each group, without including all prognosis types of PTC, such as recurrence in the thyroidectomy bed and distant metastasis. Another shortcoming of the current study is that it could not evaluate coagulation parameters in patients with different tumor stages. The postoperative lymph node metastasis was more likely if the stage before the first surgery was advanced and lateral cervical lymph node dissection was needed, which may have affected the results. A larger study population with different tumor stages would provide a higher statistical power and data on patients’ characteristics and coagulation parameters would be more homogeneous and less prone to errors.

5 Conclusion

In summary, PTC patients with different prognosis exhibited different APTTs. The shortened APTT was associated with the increased risk of SPM and postoperative cervical lymph node metastasis. The coagulation factor APTT may be associated with different PTC prognoses. Therefore, coagulation indicators such as APTT may be a new biomarker for predicting the prognosis of PTC and may provide a new molecular target for treating it, especially in combination with SPM and postoperative cervical lymph node metastasis.

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Acknowledgments

Not applicable.

  1. Funding information: The present review was supported by the Shenzhen Science and Technology Planning Project (Grant no. JYCJ20190808160011529); and the Research Foundation of Shenzhen Samii Medical Center (nos. SSMC-2020-A3 and SSMC-2021-A6).

  2. Author contributions: YHW collected the data, wrote the draft, and revised the manuscript. LYY participated in conceptualization and formal analysis. PTZ participated in drafting the article and performed study investigation and validation. XLL performed project administration and coordinated with all authors. HQL performed project design, carried out statistical analysis, participated in drafting the article, and submitted the article. HY participated in the case analysis, data collection, and project design.

  3. Conflict of interest: The authors declare that they have no competing interest.

  4. Ethics approval and consent to participate: This study was approved by the Ethical Review Board of Shenzhen Samii Medical Center (Grant no. SSMC-202103-19). Each patient signed the informed consent form and provided consent for their information to be used for medical research.

  5. Patient consent for publication: Each patient gave consent for publication. There is no patient privacy information in this article.

  6. Data availability statement: The dataset used and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Received: 2022-07-10
Revised: 2022-09-08
Accepted: 2022-09-23
Published Online: 2022-10-19

© 2022 Yanhai Wang et al., published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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https://doi.org/10.1515/chem-2022-0219
Keywords for this article
papillary thyroid carcinoma; prognosis; coagulation factors; APTT
Creative Commons
BY 4.0

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  5. Simulation of gamma-ray shielding properties for materials of medical interest
  6. Environmental impact assesment regulation applications and their analysis in Turkey
  7. Sample age effect on parameters of dynamic nuclear polarization in certain difluorobenzen isomers/MC800 asphaltene suspensions
  8. Passenger demand forecasting for railway systems
  9. Design of a Robust sliding mode controller for bioreactor cultures in overflow metabolism via an interdisciplinary approach
  10. Gamma, neutron, and heavy charged ion shielding properties of Er3+-doped and Sm3+-doped zinc borate glasses
  11. Bridging chiral de-tert-butylcalix[4]arenes: Optical resolution based on column chromatography and structural characterization
  12. Petrology and geochemistry of multiphase post-granitic dikes: A case study from the Gabal Serbal area, Southwestern Sinai, Egypt
  13. Comparison of the yield and purity of plasma exosomes extracted by ultracentrifugation, precipitation, and membrane-based approaches
  14. Bioactive triterpenoids from Indonesian medicinal plant Syzygium aqueum
  15. Investigation of the effects of machining parameters on surface integrity in micromachining
  16. The mesoporous aluminosilicate application as support for bifunctional catalysts for n-hexadecane hydroconversion
  17. Gamma-ray shielding properties of Nd2O3-added iron–boron–phosphate-based composites
  18. Numerical investigation on perforated sheet metals under tension loading
  19. Statistical analysis on the radiological assessment and geochemical studies of granite rocks in the north of Um Taghir area, Eastern Desert, Egypt
  20. Two new polypodane-type bicyclic triterpenoids from mastic
  21. Structural, physical, and mechanical properties of the TiO2 added hydroxyapatite composites
  22. Tribological properties and characterization of borided Co–Mg alloys
  23. Studies on Anemone nemorosa L. extracts; polyphenols profile, antioxidant activity, and effects on Caco-2 cells by in vitro and in silico studies
  24. Mechanical properties, elastic moduli, transmission factors, and gamma-ray-shielding performances of Bi2O3–P2O5–B2O3–V2O5 quaternary glass system
  25. Cyclic connectivity index of bipolar fuzzy incidence graph
  26. The role of passage numbers of donor cells in the development of Arabian Oryx – Cow interspecific somatic cell nuclear transfer embryos
  27. Mechanical property evaluation of tellurite–germanate glasses and comparison of their radiation-shielding characteristics using EPICS2017 to other glass systems
  28. Molecular screening of ionic liquids for CO2 absorption and molecular dynamic simulation
  29. Microwave-assisted preparation of Ag/Fe magnetic biochar from clivia leaves for adsorbing daptomycin antibiotics
  30. Iminodisuccinic acid enhances antioxidant and mineral element accumulation in young leaves of Ziziphus jujuba
  31. Cytotoxic activity of guaiane-type sesquiterpene lactone (deoxycynaropicrin) isolated from the leaves of Centaurothamnus maximus
  32. Effects of welding parameters on the angular distortion of welded steel plates
  33. Simulation of a reactor considering the Stamicarbon, Snamprogetti, and Toyo patents for obtaining urea
  34. Effect of different ramie (Boehmeria nivea L. Gaud) cultivars on the adsorption of heavy metal ions cadmium and lead in the remediation of contaminated farmland soils
  35. Impact of a live bacterial-based direct-fed microbial (DFM) postpartum and weaning system on performance, mortality, and health of Najdi lambs
  36. Anti-tumor effect of liposomes containing extracted Murrayafoline A against liver cancer cells in 2D and 3D cultured models
  37. Physicochemical properties and some mineral concentration of milk samples from different animals and altitudes
  38. Copper(ii) complexes supported by modified azo-based ligands: Nucleic acid binding and molecular docking studies
  39. Diagnostic and therapeutic radioisotopes in nuclear medicine: Determination of gamma-ray transmission factors and safety competencies of high-dense and transparent glassy shields
  40. Calculation of NaI(Tl) detector efficiency using 226Ra, 232Th, and 40K radioisotopes: Three-phase Monte Carlo simulation study
  41. Isolation and identification of unstable components from Caesalpinia sappan by high-speed counter-current chromatography combined with preparative high-performance liquid chromatography
  42. Quantification of biomarkers and evaluation of antioxidant, anti-inflammatory, and cytotoxicity properties of Dodonaea viscosa grown in Saudi Arabia using HPTLC technique
  43. Characterization of the elastic modulus of ceramic–metal composites with physical and mechanical properties by ultrasonic technique
  44. GC-MS analysis of Vespa velutina auraria Smith and its anti-inflammatory and antioxidant activities in vitro
  45. Texturing of nanocoatings for surface acoustic wave-based sensors for volatile organic compounds
  46. Insights into the molecular basis of some chalcone analogues as potential inhibitors of Leishmania donovani: An integrated in silico and in vitro study
  47. (1R,2S,5R)-5-Methyl-2-(propan-2-yl)cyclohexyl 4-amino-3-phenylbutanoate hydrochloride: Synthesis and anticonvulsant activity
  48. On the relative extraction rates of colour compounds and caffeine during brewing, an investigation of tea over time and temperature
  49. Characterization of egg shell powder-doped ceramic–metal composites
  50. Rapeseed oil-based hippurate amide nanocomposite coating material for anticorrosive and antibacterial applications
  51. Chemically modified Teucrium polium (Lamiaceae) plant act as an effective adsorbent tool for potassium permanganate (KMnO4) in wastewater remediation
  52. Efficiency analysis of photovoltaic systems installed in different geographical locations
  53. Risk prioritization model driven by success factor in the light of multicriteria decision making
  54. Theoretical investigations on the excited-state intramolecular proton transfer in the solvated 2-hydroxy-1-naphthaldehyde carbohydrazone
  55. Mechanical and gamma-ray shielding examinations of Bi2O3–PbO–CdO–B2O3 glass system
  56. Machine learning-based forecasting of potability of drinking water through adaptive boosting model
  57. The potential effect of the Rumex vesicarius water seeds extract treatment on mice before and during pregnancy on the serum enzymes and the histology of kidney and liver
  58. Impact of benzimidazole functional groups on the n-doping properties of benzimidazole derivatives
  59. Extraction of red pigment from Chinese jujube peel and the antioxidant activity of the pigment extracts
  60. Flexural strength and thermal properties of carbon black nanoparticle reinforced epoxy composites obtained from waste tires
  61. A focusing study on radioprotective and antioxidant effects of Annona muricata leaf extract in the circulation and liver tissue: Clinical and experimental studies
  62. Clinical comprehensive and experimental assessment of the radioprotective effect of Annona muricata leaf extract to prevent cellular damage in the ileum tissue
  63. Effect of WC content on ultrasonic properties, thermal and electrical conductivity of WC–Co–Ni–Cr composites
  64. Influence of various class cleaning agents for prosthesis on Co–Cr alloy surface
  65. The synthesis of nanocellulose-based nanocomposites for the effective removal of hexavalent chromium ions from aqueous solution
  66. Study on the influence of physical interlayers on the remaining oil production under different development modes
  67. Optimized linear regression control of DC motor under various disturbances
  68. Influence of different sample preparation strategies on hypothesis-driven shotgun proteomic analysis of human saliva
  69. Determination of flow distance of the fluid metal due to fluidity in ductile iron casting by artificial neural networks approach
  70. Investigation of mechanical activation effect on high-volume natural pozzolanic cements
  71. In vitro: Anti-coccidia activity of Calotropis procera leaf extract on Eimeria papillata oocysts sporulation and sporozoite
  72. Determination of oil composition of cowpea (Vigna unguiculata L.) seeds under influence of organic fertilizer forms
  73. Activated partial thromboplastin time maybe associated with the prognosis of papillary thyroid carcinoma
  74. Treatment of rat brain ischemia model by NSCs-polymer scaffold transplantation
  75. Lead and cadmium removal with native yeast from coastal wetlands
  76. Characterization of electroless Ni-coated Fe–Co composite using powder metallurgy
  77. Ferrate synthesis using NaOCl and its application for dye removal
  78. Antioxidant, antidiabetic, and anticholinesterase potential of Chenopodium murale L. extracts using in vitro and in vivo approaches
  79. Study on essential oil, antioxidant activity, anti-human prostate cancer effects, and induction of apoptosis by Equisetum arvense
  80. Experimental study on turning machine with permanent magnetic cutting tool
  81. Numerical simulation and mathematical modeling of the casting process for pearlitic spheroidal graphite cast iron
  82. Design, synthesis, and cytotoxicity evaluation of novel thiophene, pyrimidine, pyridazine, and pyridine: Griseofulvin heterocyclic extension derivatives
  83. Isolation and identification of promising antibiotic-producing bacteria
  84. Ultrasonic-induced reversible blood–brain barrier opening: Safety evaluation into the cellular level
  85. Evaluation of phytochemical and antioxidant potential of various extracts from traditionally used medicinal plants of Pakistan
  86. Effect of calcium lactate in standard diet on selected markers of oxidative stress and inflammation in ovariectomized rats
  87. Identification of crucial salivary proteins/genes and pathways involved in pathogenesis of temporomandibular disorders
  88. Zirconium-modified attapulgite was used for removing of Cr(vi) in aqueous solution
  89. The stress distribution of different types of restorative materials in primary molar
  90. Reducing surface heat loss in steam boilers
  91. Deformation behavior and formability of friction stir processed DP600 steel
  92. Synthesis and characterization of bismuth oxide/commercial activated carbon composite for battery anode
  93. Phytochemical analysis of Ziziphus jujube leaf at different foliar ages based on widely targeted metabolomics
  94. Effects of in ovo injection of black cumin (Nigella sativa) extract on hatching performance of broiler eggs
  95. Separation and evaluation of potential antioxidant, analgesic, and anti-inflammatory activities of limonene-rich essential oils from Citrus sinensis (L.)
  96. Bioactivity of a polyhydroxy gorgostane steroid from Xenia umbellata
  97. BiCAM-based automated scoring system for digital logic circuit diagrams
  98. Analysis of standard systems with solar monitoring systems
  99. Structural and spectroscopic properties of voriconazole and fluconazole – Experimental and theoretical studies
  100. New plant resistance inducers based on polyamines
  101. Experimental investigation of single-lap bolted and bolted/bonded (hybrid) joints of polymeric plates
  102. Investigation of inlet air pressure and evaporative cooling of four different cogeneration cycles
  103. Review Articles
  104. Comprehensive review on synthesis, physicochemical properties, and application of activated carbon from the Arecaceae plants for enhanced wastewater treatment
  105. Research progress on speciation analysis of arsenic in traditional Chinese medicine
  106. Recent modified air-assisted liquid–liquid microextraction applications for medicines and organic compounds in various samples: A review
  107. An insight on Vietnamese bio-waste materials as activated carbon precursors for multiple applications in environmental protection
  108. Antimicrobial activities of the extracts and secondary metabolites from Clausena genus – A review
  109. Bioremediation of organic/heavy metal contaminants by mixed cultures of microorganisms: A review
  110. Sonodynamic therapy for breast cancer: A literature review
  111. Recent progress of amino acid transporters as a novel antitumor target
  112. Aconitum coreanum Rapaics: Botany, traditional uses, phytochemistry, pharmacology, and toxicology
  113. Corrigendum
  114. Corrigendum to “Petrology and geochemistry of multiphase post-granitic dikes: A case study from the Gabal Serbal area, Southwestern Sinai, Egypt”
  115. Corrigendum to “Design of a Robust sliding mode controller for bioreactor cultures in overflow metabolism via an interdisciplinary approach”
  116. Corrigendum to “Statistical analysis on the radiological assessment and geochemical studies of granite rocks in the north of Um Taghir area, Eastern Desert, Egypt”
  117. Corrigendum to “Aroma components of tobacco powder from different producing areas based on gas chromatography ion mobility spectrometry”
  118. Corrigendum to “Mechanical properties, elastic moduli, transmission factors, and gamma-ray-shielding performances of Bi2O3–P2O5–B2O3–V2O5 quaternary glass system”
  119. Erratum
  120. Erratum to “Copper(ii) complexes supported by modified azo-based ligands: Nucleic acid binding and molecular docking studies”
  121. Special Issue on Applied Biochemistry and Biotechnology (ABB 2021)
  122. Study of solidification and stabilization of heavy metals by passivators in heavy metal-contaminated soil
  123. Human health risk assessment and distribution of VOCs in a chemical site, Weinan, China
  124. Preparation and characterization of Sparassis latifolia β-glucan microcapsules
  125. Special Issue on the Conference of Energy, Fuels, Environment 2020
  126. Improving the thermal performance of existing buildings in light of the requirements of the EU directive 2010/31/EU in Poland
  127. Special Issue on Ethnobotanical, Phytochemical and Biological Investigation of Medicinal Plants
  128. Study of plant resources with ethnomedicinal relevance from district Bagh, Azad Jammu and Kashmir, Pakistan
  129. Studies on the chemical composition of plants used in traditional medicine in Congo
  130. Special Issue on Applied Chemistry in Agriculture and Food Science
  131. Strip spraying technology for precise herbicide application in carrot fields
  132. Special Issue on Pharmacology and Metabolomics of Ethnobotanical and Herbal Medicine
  133. Phytochemical profiling, antibacterial and antioxidant properties of Crocus sativus flower: A comparison between tepals and stigmas
  134. Antioxidant and antimicrobial properties of polyphenolics from Withania adpressa (Coss.) Batt. against selected drug-resistant bacterial strains
  135. Integrating network pharmacology and molecular docking to explore the potential mechanism of Xinguan No. 3 in the treatment of COVID-19
  136. Chemical composition and in vitro and in vivo biological assortment of fixed oil extracted from Ficus benghalensis L.
  137. A review of the pharmacological activities and protective effects of Inonotus obliquus triterpenoids in kidney diseases
  138. Ethnopharmacological study of medicinal plants in Kastamonu province (Türkiye)
  139. Protective effects of asperuloside against cyclophosphamide-induced urotoxicity and hematotoxicity in rats
  140. Special Issue on Essential Oil, Extraction, Phytochemistry, Advances, and Application
  141. Identification of volatile compounds and antioxidant, antibacterial, and antifungal properties against drug-resistant microbes of essential oils from the leaves of Mentha rotundifolia var. apodysa Briq. (Lamiaceae)
  142. Phenolic contents, anticancer, antioxidant, and antimicrobial capacities of MeOH extract from the aerial parts of Trema orientalis plant
  143. Chemical composition and antimicrobial activity of essential oils from Mentha pulegium and Rosmarinus officinalis against multidrug-resistant microbes and their acute toxicity study
  144. Special Issue on Marine Environmental Sciences and Significance of the Multidisciplinary Approaches
  145. An insightful overview of the distribution pattern of polycyclic aromatic hydrocarbon in the marine sediments of the Red Sea
  146. Antifungal–antiproliferative norcycloartane-type triterpenes from the Red Sea green alga Tydemania expeditionis
  147. Solvent effect, dipole moment, and DFT studies of multi donor–acceptor type pyridine derivative
  148. An extensive assessment on the distribution pattern of organic contaminants in the aerosols samples in the Middle East
  149. Special Issue on 4th IC3PE
  150. Energetics of carboxylic acid–pyridine heterosynthon revisited: A computational study of intermolecular hydrogen bond domination on phenylacetic acid–nicotinamide cocrystals
  151. A review: Silver–zinc oxide nanoparticles – organoclay-reinforced chitosan bionanocomposites for food packaging
  152. Green synthesis of magnetic activated carbon from peanut shells functionalized with TiO2 photocatalyst for Batik liquid waste treatment
  153. Coagulation activity of liquid extraction of Leucaena leucocephala and Sesbania grandiflora on the removal of turbidity
  154. Hydrocracking optimization of palm oil over NiMoO4/activated carbon catalyst to produce biogasoline and kerosine
  155. Special Issue on Pharmacology and metabolomics of ethnobotanical and herbal medicine
  156. Cynarin inhibits PDGF-BB-induced proliferation and activation in hepatic stellate cells through PPARγ
  157. Special Issue on The 1st Malaysia International Conference on Nanotechnology & Catalysis (MICNC2021)
  158. Surfactant evaluation for enhanced oil recovery: Phase behavior and interfacial tension
  159. Topical Issue on phytochemicals, biological and toxicological analysis of aromatic medicinal plants
  160. Phytochemical analysis of leaves and stems of Physalis alkekengi L. (Solanaceae)
  161. Phytochemical and pharmacological profiling of Trewia nudiflora Linn. leaf extract deciphers therapeutic potentials against thrombosis, arthritis, helminths, and insects
  162. Pergularia tomentosa coupled with selenium nanoparticles salvaged lead acetate-induced redox imbalance, inflammation, apoptosis, and disruption of neurotransmission in rats’ brain
  163. Protective effect of Allium atroviolaceum-synthesized SeNPs on aluminum-induced brain damage in mice
  164. Mechanism study of Cordyceps sinensis alleviates renal ischemia–reperfusion injury
  165. Plant-derived bisbenzylisoquinoline alkaloid tetrandrine prevents human podocyte injury by regulating the miR-150-5p/NPHS1 axis
  166. Network pharmacology combined with molecular docking to explore the anti-osteoporosis mechanisms of β-ecdysone derived from medicinal plants
  167. Chinese medicinal plant Polygonum cuspidatum ameliorates silicosis via suppressing the Wnt/β-catenin pathway
  168. Special Issue on Advanced Nanomaterials for Energy, Environmental and Biological Applications - Part I
  169. Investigation of improved optical and conductivity properties of poly(methyl methacrylate)–MXenes (PMMA–MXenes) nanocomposite thin films for optoelectronic applications
  170. Special Issue on Applied Biochemistry and Biotechnology (ABB 2022)
  171. Model predictive control for precision irrigation of a Quinoa crop
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