The early biomarker of immature granulocyte count in predicting right-side colonic complicated acute diverticulitis: a retrospective cohort study (2024)

  • Qi Su1,
  • Qingzhi Wang2 &
  • Yantian Cao2

BMC Gastroenterology volume24, Articlenumber:351 (2024) Cite this article

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Abstract

Objective

Early identification of complicated acute diverticulitis(cAD) is especially significant for clinical physician and surgeon to reduce the antibiotic usage and the risk of emergency surgery. This study was aimed to investigate the significance of immature granulocyte(IG) count in early prediction for right-side(Rt-side) cAD.

Methods

The patients with Rt-side colonic acute diverticulitis was enrolled between January, 2019 and March, 2024, and divided into complicated and simple acute diverticulitis group(cAD and sAD). The data about demographic, clinical and laboratory parameters were collected and compared. Logistic regression analysis and receiver operator characteristic(ROC) curves were used to assess the predictive values of these parameters for Rt-side complicated diverticulitis.

Results

289 participants who met the inclusion criteria were followed as 31 patients in cAD group and 258 in sAD group. Compared to sAD group, cAD group had the higher body mass index(BMI) and peripheral blood routine parameters, especially IG count, systemic immune inflammation index(SII) and neutrophil-to-lymphocyte ratio(NLR), with the statistically significant differences(P<0.001). Moreover, logistic regression analysis indicated that IG count was a significant and independent predictors for cAD(OR 4.92, 95%CI 3.86–8.39). In the ROC analysis, area under the ROC curves (AUC) was found for IG count(0.93(95%CI 0.88–0.99) ) and SII(0.88(95%CI 0.820–0.95)). The optimal cut-off value of IG count was 0.10 with the largest sensitivity of 80.60% and specificity of 100.00% for identifying Rt-side colonic complicated diverticulitis.

Conclusion

IG count was a more comparable and independent predictor for Rt-side colonic complicated diverticulitis with a largest AUC than other markers in complete blood count (CBC). Given its early arise, easy accessibility and no-radiation, it can largely convince physicians’ decision-making of antibiotic abuse and surgeons’ early intervention in Rt-side colonic cAD.

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Introduction

Colonic acute diverticulitis(AD) is characterized by an acute inflammation in weak site of the bowel wall and micro-perforation of diverticulum. Its prevalence appears to be generally higher in the left colon in Western countries [1]. Conversely, in Asia, it predominantly occurs in right-side(Rt-side) colon with 38-75%, which extremely easily confused with acute appendicitis in the General surgery departments [2, 3]. Of those who had Rt-side colonic acute diverticulitis, approximately 12-15% suffered one or more associated complications of bowel obstruction, stricture, abscess, fistula, or perforation [4]. They are usually defined as complicated acute diverticulitis(cAD), even though its incidence was lower than among left-side colonic AD, reported by a meta-analysis [5]. Low clinical suspicion about cAD leads to persistently high mortality rate of up to 5% due to severe complications over the past decades [6, 7], which can be improved by early and timely surgical intervention. Meanwhile, it was equally important for reducing the antibiotic abuse in patients with simple acute diverticulitis(sAD). Consequently, it remains to be an enormous challenge for early and quick identification of complicated diverticulitis in clinic.

Peripheral blood routine test currently has been considered as an easily acquired and quick options for assessing severity of infectious diseases. In which, many parameters of white blood cells(WBC), neutrophils(NEU) and monocyte distribution width(MDW), and its derived indicators of neutrophil-to-lymphocyte ratio(NLR) and platelet-to-lymphocyte ratio(PLR) have been suggested to predict complicated diverticulitis [8,9,10,11]. Besides that, in recent years, immature granulocytes (IG), namely the precursor of WBC, can be detected in peripheral whole blood earlier than WBC and NEU under the infection, inflammation, sepsis, and other stimuli conditions. And a number of studies had already suggested that IG count had the earlier prognostic value in patients whether with acute pancreatitis or acute complicated appendicitis [12, 13]. Unfortunately, no study has focused on the accuracy of the IG count in diagnosing Rt-side colonic complicated diverticulitis, and its predicted state remain unclear.

IG count may be a novel screening biomarker for identifying complicated diverticulitis. In this retrospective study, we investigated the predictive significance of IG count in patients with Rt-side colonic cAD.

Materials and methods

Study design and patient selection

The whole patients enrolled were from the Third Affiliated Hospital of Xinxiang Medical University between January 2019 and March 2024. Data were extracted retrospectively from institutional electronic medical recording system.

This study was approved by the Ethics Committee of the Third Affiliated Hospital of Xinxiang Medical University. And written informed consent from patients was waived by Ethical committee of the Third Affiliated Hospital of Xinxiang Medical University due to its retrospective nature. This study was in accordance with the ethical standards of the Institutional Committee and regulations of nation.

Patients with a diagnosis of colonic acute diverticulitis by abdominal computed tomography(CT) were included. Inclusion criteria for this study was as follows: (1) ages ranged from 18 to 80 years old, (2) located in Rt-side colon, (3) first episode of colonic diverticulitis, (4) indicated blood samples were obtained at the initial admission before any intervention. The exclusion criteria was: (1) combined with other active infectious disease, (2) patients with hematological diseases, pregnancy status and children, (3) already or currently receiving specific treatment that will alter the leukocyte count(e.g. antibiotic) before whole blood cell test, (4) colonic tumors confirmed by colonoscopy finally. Any disagreement in this process was resolved by consensus(Yantian Cao and Qi Su).

Data selection

The study population was divided into two groups as those who would diagnosed with complicated acute diverticulitis(cAD) based on CT(such as bowel obstruction, stricture, abscess, fistula, or perforation), and those that had no complications(simple acute diverticulitis(sAD)). And the demographics(age, gender, BMI, favor of smoking and alcohol), clinical characteristics(onset time of AD, comorbidities, location of diverticulitis), and laboratory parameters (WBC, NEU, lymphocytes, platelets(PLT), IG count) were directedly recorded, as well as systemic immune inflammation index(SII), NLR, PLR, platelet-to-neutrophil ratio (PNR) were manually calculated. The statistical differences between two groups were analyzed.

Statistical analysis

The variables between two groups were analyzed by using variance (ANOVA) for continuous variables and reported as median plus or minus standard deviation(M ± SD), and Chi-squared test for categorical variables expressed as numbers(percentage). Univariable and multivariable binary regression analysis were used to analyze the risk odds(OR) of IG counts, SII, WBC and BMI among cAD group. Receiver operator characteristic(ROC) curves and area under the ROC curves(AUC) were used as diagnostic tests to evaluate the accuracy of IG count, SII and NLR as the predictors of cAD, Based on the Youden index [14] calculated by sensitivity(Sen) (%) plus specificity(Spe) (%) minus one, the point of cut-off value was performed to distinguish complicated diverticulitis from simple diverticulitis. Furthermore, likelihood ratio(LR) can also be used to evaluate diagnostic test performance, which contains positive likelihood ratio(LR + = Sen /(1-Spe) and negative likelihood ratio(LR- =(1-Sen)/Spe) [15]. The value of P < 0.05 was considered statistically significant. SPSS 24.0 was used for all comparisons and the statistical analyses.

Results

Patients’ characteristics

Among 318 patients who were diagnosed as acute colonic diverticulitis, 289 of them complied with study inclusion criteria and was included into our study, 31 had colonic complicated diverticulitis and 258 had simple diverticulitis (Fig.1). All of patients had Rt-side colonic diverticulitis: among cAD group, 9 in the cecum, 15 in the ascending colon, and 7 in both of cecum and ascending colon; among sAD group, 95 in the cecum, 78 in the ascending colon, and 85 in both of cecum and ascending colon. In comparison to sAD group, the mean age was 49.97 years and 67.74% of the patients were male in cAD group without statistical differences(P > 0.05). And no statistical difference was also observed between two groups in terms of favor of smoking(17 vs. 120), alcohol(19 vs. 127), and onset time of disease(hours, 41.87 vs. 35.54). By contrast, BMI, levels of WBC, NEU, IG count and values of SII, NLR, PLR, PNR in cAD group were significantly higher than in sAD group(P<0.001), while lymphocyte in cAD group was lower than sAD(P<0.001). Table1 summarized the patients’ demographics data and the results of clinical characteristics and baseline laboratory parameters.

The flowchart of the enrolled study patients

Full size image
Full size table

Logistic regression analysis

On univariable binary logistic regression analysis, we found BMI showed a significant correlation with cAD(OR 1.19, 95%CI 1.09–1.31, P<0.001) (Table2).

Full size table

And in multivariable binary logistic regression analysis, WBC and IG count had the positive correlations with cAD(OR 1.41 95%CI 1.11–1.80, P<0.05, OR 4.92 95%CI 3.86–8.39, P<0.05, respectively). However, SII was not significantly correlated with cAD(OR 1.00) (Table2).

ROC curve and AUC analysis

We performed ROC curve and calculated AUC for laboratory parameters to predict the independent risk factors and optimal biomarker among cAD population. As the Fig.2 revealed, the AUC values were as follows in descending order: IG count, 0.93(95%CI 0.88–0.99); SII, 0.88(95%CI 0.82–0.95); NLR, 0.87(95%CI 0.81–0.93); PLR, 0.82(95%CI 0.76–0.88); WBC, 0.80(95%CI 0.69–0.90) and NEU, 0.78(95%CI 0.67–0.89), respectively. Furthermore, based on the Youden index calculated, the cut-off value of IG count was 0.10(95%CI 0.88–0.99) with the optimal Sen(80.60%), Spe (100.00%), LR+(0.00) and LR-(0.19) (Table3).

ROC curves for IG and other inflammatory biomarkers(SII, NLR, PLR, WBC, NEU

Full size image
Full size table

Discussion

This is the currently first clinical retrospective study to evaluate the accuracy of IG count in predicting Rt-side colonic complicated acute diverticulitis. It concluded that the high level of IG count, WBC and BMI were the independent risk factors. And IG count had been identified as the largest AUC of 0.93 with the optimal sensitivity(80.60% ) and specificity (100.00%).

In brief, IG count can be considered as an novel alternative to identify Rt-side colonic complicated diverticulitis and guide the clinical treatment decision. A meta-analysis of S Hajibandeh et.al [5] enrolled nine studies of 2933 patients and suggested that the risk of complicated diverticulitis in the Rt-side colon was lower than in left-side colon(OR 0.21 (0.08, 0.55), P = 0.001). Thus the antibiotic utilization rate should be lower in Rt-side colonic cAD, at least theoretically, the antibiotic usage was even in no sense in most cases of uncomplicated diverticulitis. In reality, antibiotic abuse still faces significant challenges in worldwide [16]. Surprisingly, IG count can be a promising alternative biomarker to decide antibiotic treatment selectively rather than routinely. Furthermore, compared to patients suffering simple AD, the high mortality of patients with complicated AD still continuously puzzled the clinical surgeons [6]. The early predictor of IG count, larger than 0.10*109/L, can be a warning signal of complicated AD to warn surgeons for surgical intervene as soon as possible. Of course, beyond all doubt, abdominal CT scan is the most effective option for diagnosing complicated acute diverticulitis [17]. Nonetheless, the presents of imaging(such as micro-perforates, small abscesses)were latter than the increase of inflammatory cells in CBC tests. Additionally, the high expenditure of $ 98.58 at 128 CT scan increased the financial burden compared to CBC cost of $ 4.23. CT scan was also limited in certain population and circumstances, such as pregnant women, children, as well as the area of lacking imaging equipment. Considering these dilemma, it is possible to be identified as complementary option to early identifying complicated diverticulitis.

Compared to inflammatory biomarkers, such as WBC, NEU and PLT, IG count has own unique advantages. As we all know, the increase of IG count in peripheral blood indicates activation of bone marrow. It can be generally detected preceding leukocytosis in peripheral blood in response to infection and inflammation [18, 19]. In a series of clinical studies, IG count was considered as an early and effective biomarker in determining the severity of inflammatory events, such as acute appendicitis, acute pancreatitis and sepsis [20,21,22]. Our study also supposed that IG count had the predictive value of Rt-side colonic complicated diverticulitis. In addition to preventing deferment of complications, its time of testing process and report out of IG count was shorter than of some biochemistry parameters, such as C-reactive protein(CRP) and procalcitonin (PCT), even if they had the certain values in discriminating complicated from uncomplicated diverticulitis [23]. And the additional costs of CRP and PCT also required attention. Similarly to IG count, MDW was a relatively early marker in predicting complicated diverticulitis, as Chang et al.(2023) [8] found. Unfortunately, MDW had the smaller AUC of 0.870 and lower specificity of 80.6% than IG count, and it suggested that the left-side colonic complicated diverticulitis was the risk factor, which differed from our objective locating in Rt-side colon.

SII was another elevated parameter in cAD. SII was calculated as the neutrophil counts (*109/L) multiplied by the platelet counts (*109/L) and divided by the lymphocyte counts (*109/L).As a combinated parameter of estimating the inflammatory severity of diseases, it can easily form consensus and avoid the limitations of single indicators, whatever WBC or CRP. As previous study reported, SII was considered as an effective marker for predicting prognosis of colorectal cancer and identifying severe acute pancreatitis [24, 25]. However, few study was about the efficacy of the SII in detecting acute complicated diverticulitis. Our study demonstrated that if value of SII was greater than 1521.24(*109/L)(cut-off value) in patients with Rt-side colonic diverticulitis, it indicted as the complicated diverticulitis. So IG count maybe serve as an useful supplement to single role of neutrophil count and platelet count.

The predicting value of NLR, another combinated parameter, was next only to SII in our study. It was calculated by the neutrophil count divided by lymphocyte count. As a reliable parameter, it already has been routinely used by distinguish of benign and malignant diseases. In particular, the high levels of NLR (cut-off value, 5.40) were associated with shorter intervals between episodes of acute diverticulitis, a higher number of readmissions, and longer hospital stay in diverticulitis [26]. This was comparable to the results of our study(cut-off value, 5.70). However, NLR had lower accuracy than WBC count for diagnosing complications of colonic diverticulitis, published by Reynolds I et al. [27], which was different from our finding(AUC NLR vs. WBC: 0.87 vs. 0.80). This can be explained that NLR might be closely related to immune response of studied population [28]. Thus NLR can be preserved as an auxiliary parameter for diagnosing complicated diverticulitis, which cannot be verified on the basis of abdominal CT scan.

There were some limitations in this study. First, this study performed at the single center with the small sample, especially the numbers in the cAD group(31 cases), which resulted to poor evidence and the risk of overfitting in regression analyses, more multicenter studies with large sample size can solve it. Second, due to retrospective nature of study, some data was not able to be measured, such as the results of colonoscopy, single or multiple number of diverticula. Thus, they might impact the results of multivariate binary regression analysis. Third, in terms of epidemiological characteristics of colonic diverticulitis in Asia, the only data from cases of Rt-side colonic diverticulitis from our hospital were extracted and analyzed. Besides, most of references cited among our study were limited in right-side colon, which is a paradox in analyzing the differences of predicting markers. So more clinical studies is needed whether our results about the accuracy of IG count is applicable to left-side colonic diverticulitis. Finally, it was too incomplete for data about IG count over onset time to analyze dynamically.

Conclusions

Our study demonstrated IG count was determined to be superior diagnostic biomarker for complicated diverticulitis in early stage. When cut-off value was 0.10, it showed an optimal sensitivity of 80.60% and specificity of 100.00%. The significance of IG count comes to the fore, while more clinical studies are needed to further verified in future.

Data availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Abbreviations

AD:

Colonic acute diverticulitis

cAD:

Complicated acute diverticulitis

sAD:

Simple acute diverticulitis

Rt-side:

Right-side

CBC:

Complete blood count

WBC:

White blood cells

NEU:

Neutrophils

MDW:

Monocyte distribution width

NLR:

Neutrophil-to-lymphocyte ratio

PLR:

Platelet-to-lymphocyte ratio

IG:

Immature granulocyte

PLT:

Lymphocytes, platelets

PNR:

Platelet-to-neutrophil ratio

ROC:

Receiver operator characteristic

AUC:

Area under the ROC curves

Sen:

Sensitivity

Spe:

Specificity

LR+:

Positive likelihood ratio

LR-:

Negative likelihood ratio

BMI:

Body mass index

SII:

Systemic immune inflammation index

NLR:

Neutrophil-to-lymphocyte ratio

CT:

Computed tomography

OR:

Odds ratio

CRP:

C-reactive protein

PCT:

Procalcitonin

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Acknowledgements

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Funding

This study has been supported by grant of Henan Provincial Science and Technology Research Project(No. LHGJ20210547).

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Authors and Affiliations

  1. Department of General surgery, The Third Affiliated Hospital of Xinxiang Medical University, Hualan Avenue, Xinxiang, 453003, Henan Province, China

    Qi Su

  2. Department of Gastroenterology, The Third Affiliated Hospital of Xinxiang Medical University, Hualan Avenue, Xinxiang, 453003, Henan Province, China

    Qingzhi Wang&Yantian Cao

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Contributions

Y. C. participated in the design of the study, collection and analyze of data, and drafted the original manuscript. Q. S. participated in the collection of data and performed the statistical analysis. Q. W. participated in the revision of manuscript and supervision of all process. All authors read the final manuscript and approved the submission .

Corresponding author

Correspondence to Yantian Cao.

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Ethics approval and consent to participate

This study was approved by the Ethics Committee of the Third Affiliated Hospital of Xinxiang Medical University. And written informed consent from patients was waived by Ethical committee of the Third Affiliated Hospital of Xinxiang Medical University due to its retrospective nature. This study was in accordance with the ethical standards of the Institutional Committee and regulations of nation.

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The authors declare no competing interests.

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The early biomarker of immature granulocyte count in predicting right-side colonic complicated acute diverticulitis: a retrospective cohort study (3)

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Su, Q., Wang, Q. & Cao, Y. The early biomarker of immature granulocyte count in predicting right-side colonic complicated acute diverticulitis: a retrospective cohort study. BMC Gastroenterol 24, 351 (2024). https://doi.org/10.1186/s12876-024-03443-0

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Keywords

  • Complicated acute diverticulitis
  • Right-side colon
  • Immature granulocyte count
  • Systemic immune inflammation index
  • Neutrophil-to-lymphocyte ratio
The early biomarker of immature granulocyte count in predicting right-side colonic complicated acute diverticulitis: a retrospective cohort study (2024)
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