Neutrophil-to-lymphocyte ratio as a predictor of intestinal resection in incarcerated inguinal hernias

Perez R.D.; Villena M.A.; Zavaleta-Corvera C.; Caballero-Alvarado J.; Zafra Ch.; Pozzuoli G.

doi:https://doi.org/10.17116/hirurgia202401151

Introduction

An inguinal hernia is defined as a protrusion or projection of an organ, or part of it, into an abnormal opening in the inguinal canal [1]. Its appearance depends on any factor that increases intra-abdominal pressure such as chronic cough, COPD and constipation [2, 3, 4]. The prevalence of inguinal hernia is 5% to 10%; of which, 0.3% are incarcerated, 0.3% to 2.9% being strangled [5, 6].

Among the various classifications of this pathology, they can be according to the anatomical repairs: direct, indirect and femoral; or according to the clinical presentation: reducible, irreducible incarcerated and irreducible strangled [7]. Kurt et al., reports that 15% of patients with incarcerated inguinal hernia need intestinal resection [8]. Alvarez et al., reported that femoral hernias cause 57% of intestinal strangulations, of which 41% required intestinal resection, therefore, they consider that the pathology increases the morbidity and mortality rate [9, 10].

The incarcerated hernia is the consequence of continuous inflammation of the hernial sac that prevents the return of the herniated structure to its place of origin, causing damage to the venous return and lymphatic system of the viscera. On the other hand, a strangulated hernia is due to progressive and permanent compression, which affects total arterial circulation, producing ischemia and/or necrosis that can even lead to peritonitis [11, 12]. The neutrophil-to-lymphocyte ratio (NLR) is an easily accessible inflammatory biomarker obtained from blood cell counts. It is determined from the ratio of neutrophils to lymphocytes and turns out to be very useful in predicting severity in patients with pathologies that present inflammation [13, 14]. This type of pathology needs emergency treatment and the technique to be chosen should seek the reduction and reintroduction of the herniated structure, providing optimal exposure in cases of intestinal resection avoiding sequelae, recurrences, less postoperative pain, and rapid integration into daily activities [15].

The aim of this study is to determine whether the neutrophil-to-lymphocyte ratio (NLR) predicts bowel resection of incarcerated hernias based on the neutrophil-to-lymphocyte ratio (NLR).

Material and method

Study area

The study was carried out at the Belen Hospital of Trujillo. The investigation was carried out in the period January 2013 — August 2019 in the Surgery service in the Department of General Surgery and Emergency Surgery and Critical Care.

Population and sample

An observational, analytical, diagnostic test and retrospective study was carried out. The study population consisted of patients diagnosed with unilateral inguinal hernia with obstruction. The sample size calculation was found using the statistical formula for diagnostic tests with a sensitivity of 86%, where p=0.20. In this way, a sample of 161 patients was obtained, including patients with incarcerated or strangulated inguinal hernia, older than 18 years, of both sexes, who have complete medical records and blood counts on admission; and pregnant women, patients with peritonitis or intra-abdominal infection due to a cause other than inguinal hernia pathology, patients diagnosed with: HIV, hepatitis B and C, coagulopathies or chronic diseases that require use with corticosteroids or immunosuppressants that alter the leukocyte ratio were excluded, and patients do not have complete medical records.

Definitions-Measurements

Incarcerated inguinal hernia is defined as a hernia with obstruction that does not reduce. The strangulated inguinal hernia is the hernia with irreducible obstruction that impairs the total arterial circulation of the incarcerated organ. Intestinal resection is the removal of all or part of the small or large intestine due to loss of its viability [16]. The neutrophil-to-lymphocyte ratio index obtained from the division of the neutrophil count by the lymphocyte count [17]. The platelet-to-lymphocyte ratio obtained from the division of the neutrophil count by the lymphocyte count [18]. Other variables were included: sex, age, type of hernia, side of hernia, intestinal obstruction, duration of incarceration >24 hours, and red blood cell distribution width (RDW).

Procedures

This study has the approval of the School of Human Medicine of the Antenor Orrego Private University and the Surgery Service of the Belen Hospital of Trujillo. The medical records were selected by simple random sampling of patients who underwent surgical repair with a diagnosis of inguinal hernia with obstruction from January 2013 to August 2019 and who met the selection criteria. The information obtained was recorded in a data collection form, to later be transferred to an Excel database in order to carry out the statistical analysis.

Statistic analysis

The data was analyzed using the statistical software SPSS v. 25, which will allow obtaining the information through double entry tables. The mean, central deviation, frequency and percentages that are presented in simple tables were calculated. For the relationship between the event and the exposure, it was analyzed using Chi square (χ²) and T-Student. Associations are significant if <5%, with 95% CI. The sensitivity, specificity, positive predictive value, negative predictive value of the neutrophil-to-lymphocyte ratio index were found. Likewise, the area under the ROC curve was calculated to determine the predictive accuracy and find a better cut-off point that demonstrates greater sensitivity and specificity.

Ethical aspects

The study has the approval of the Research and Ethics Committee of the Antenor Orrego Private University under resolution No. 1167 — 2019-FMEHU-UPAO. Due to the fact that it was a retrospective investigation, in which only data from clinical histories were obtained, the International Ethical Guidelines for Biomedical Research in Human Beings [19] and the principles of the Declaration of Helsinki [20].

Results

The frequency of bowel resection in 161 patients with incarcerated inguinal hernias was 20 patients (12.4%), while 141 did not undergo resection (87.6%). Variables such as sex, type of hernia, side of the hernia, intestinal obstruction and duration of incarceration >24 hours were considered, presenting these last 2 statistically significant associations with intestinal resection (p=0.007 and p=0.048 respectively) in the Chi-square test (Table 1).

Table 1. Association of intestinal resection in patients with incarcerated inguinal hernias at the Belen Hospital of Trujillo

Intervening variables		Intestinal resection				Total (%)		p
		yes		no
		frequency (n=20)	% (12.4%)	frequency (n=141)	% (87.6%)
Sex	Female	6	30.0	33	23.4	39	24.2	0.519
Sex	Male	14	70.0	108	76.6	122	75.8	0.519
Type of hernia	Indirect	13	65.0	73	51.8	86	53.4	0.267
Type of hernia	Direct	7	35.0	68	48.2	75	46.6	0.267
Side of hernia	Right	14	70.0	83	58.9	97	60.2	0.341
Side of hernia	Left	6	30.0	58	41.1	64	39.8	0.341
Intestinal obstruction	Yes	20	100.0	102	72.3	122	75.8	0.007
Intestinal obstruction	No	0	0.0	39	27.7	39	24.2	0.007
Duration of incarceration >24 hours	Yes	12	60.0	52	36.9	64	39.8	0.048
Duration of incarceration >24 hours	No	8	40.0	89	63.1	97	60.2	0.048
Total		20	100.0	141	100.0	161	100.0

Note. Pearson’s c², p<0.05 signficant. *Source: Belen Hospital of Trujillo — Medical Records Archive, January 2013 — August 2019.

For this reason, a multivariate analysis of these last variables was carried out; age, red blood cell distribution width (RDW) and platelet/lymphocyte (PLT/L) in which the patients who underwent resection showed that age and PLT/L (264.66±160.83 vs 161.21±56.78) had higher values in relation to the group without resection (p=0.020 and p=0.010, respectively), according to the T-Student test (Table 2).

Table 2. Association of intestinal resection in patients with incarcerated inguinal hernias at the Belen Hospital of Trujillo

Intervening variables	Intestinal resection				p
	yes = 20		no = 141
	mean	standard deviation	mean	standard deviation
Age	69	16	60	17	0.020
RDW	44.07	3.72	44.34	6.58	0.861
PLT/L	264.66	160.83	161.21	56.78	0.010

Note. T-Student, p<0.05 signficant, RDW: red blood cell distribution width, PLT/L: platelets/lymphocytes. *Source: Belen Hospital of Trujillo — Medical Records Archive, January 2013 — August 2019.

Thus, the NLR >6.5 is taken as a predictor of intestinal resection in patients with incarcerated hernias, it shows the sensitivity, specificity, positive predictive value, negative predictive value, likelihood ratio (+) and similarity (–) of 75%, 93.62%, 62.5%, 96.35%, 11.75 and 0.27, respectively (Table 3).

Table 3. Sensitivity, specificity, positive predictive value, negative predictive value, likelihood ratio (+), likelihood ratio (–) in the prediction of intestinal resection in incarcerated hernias

NLR	Intestinal resection		Total
NLR	yes	no	Total
>6.5	15	9	24
≤6.5	5	132	137
Total	20	141	161

Note. Sensitivity = 75%; specificity = 93.62%; positive predictive value = 62.5%; negative predictive value = 96.35%; likelihood ratio (+) = 11.75; likelihood ratio (–) = 0.27. *Source: Belen Hospital of Trujillo — Medical Records Archive, January 2013 — August 2019.

Thereby the curve for diagnostic tests ROC (Receiver operating characteristic curve) is created. The curve is observed, it demonstrates the diagnostic accuracy of the neutrophil-to-lymphocyte ratio, it shows an area under the curve of 0.94 [0.879—0.969] (Graph). Based on the ROC curve, the neutrophil-to-lymphocyte ratio index >5.14 is presented as the optimum cut-off point as a predictor of intestinal resection in patients with incarcerated hernias (Table 4).

ROC curve analysis of NLR as a predictor of intestinal resection

ROC (Receiver operating characteristic curve). Area under the curve. NLR=0.94. *Source: Belen Hospital of Trujillo — Medical Records Archive, January 2013 — August 2019.

Table 4. Optimal cut-off point of the neutrophil-to-lymphocyte ratio as a predictor of intestinal resection in patients with incarcerated hernias

Positive if greater than or equal to^a	Sensitivity	1-Specificity	Specificity
4.700	0.900	0.191	0.809
4.820	0.900	0.184	0.816
4.895	0.900	0.177	0.823
4.935	0.900	0.170	0.830
5.020	0.900	0.163	0.837
5.140	0.900	0.156	0.844
5.270	0.850	0.156	0.844
5.370	0.800	0.156	0.844
5.430	0.800	0.149	0.851
5.480	0.750	0.149	0.851
5.580	0.750	0.142	0.858

Note. *Source: Belen Hospital of Trujillo — Medical Records Archive, January 2013 — August 2019.

The diagnostic performance with the best cut-off point: NLR >5.14, obtained from the ROC curve, to predict intestinal resection, shows a sensitivity, specificity, likelihood ratio (+) and likelihood ratio (–) of 90%, 84.4%, 45%, 98.35%, 5.77 and 0.12, respectively (Table 5).

Table 5. Sensitivity, specificity, positive predictive value, negative predictive value, likelihood ratio (+), likelihood ratio (–) in the prediction of intestinal resection in incarcerated hernias (5.14 cut-off)

NLR	Intestinal resection		Total
NLR	yes	no	Total
≥5.14	18	22	40
<5.14	2	119	121
Total	20	141	161

Note. Sensitivity = 90%; specificity = 84.4%; positive predictive value = 45%; negative predictive value = 98.35%; likelihood ratio (+) = 5.77; likelihood ratio (–) = 0.12. *Source: Belen Hospital of Trujillo — Medical Records Archive, January 2013 — August 2019.

Discussion

Inguinal hernia surgeries continue to be a frequent problem within general surgery procedures [21]. Inguinal hernia is the third leading cause of care for gastrointestinal problems [22], finding that 5% to 15% of patients undergo emergency surgery due to complications, hernia incarceration and strangulation being more frequent [23]. Action must be taken in the shortest possible time to prevent inguinal hernias from incarcerating the hernial content and later leading to strangulation, requiring resection of the affected segment. Therefore, it is essential to find low-cost diagnostic tools and good access for medical personnel.

White line biomarkers allow early identification of an acute inflammatory response. The systemic inflammatory response has been shown to be a prognostic marker in different types of cancers. A great relationship has been found with leukocytosis, monocytosis, increased the neutrophil-to-lymphocyte ratio (NLR) and increased platelet/lymphocyte (PLT/L) as prognostic markers [24, 25]. The neutrophil-to-lymphocyte ratio (NLR) are easily accessible indicators to determine the state of the inflammatory response. For this reason, this indicator is used as a predictive marker in inflammatory and infectious pathologies and is useful in complications that can cause death [26, 27, 28].

Regarding our research, incarcerated hernia was more frequent in men older than 60 (p<0.05), as can be verified in Primatesta and Goldacre [29], Italy, which admitted 28,399 patients undergoing inguinal hernia surgery. It was observed that 9% of admissions were emergency, being more frequent in men, increasing the incidence rate in people older than 50 years. For this reason, de Goede et al. [30], in Rotterdam, conducted a 20-year cohort study to determine the risk factors for inguinal hernia in men older than 45 years. However, Kurt et al. [8], in a retrospective study carried out in Turkey, agrees that being older than 65 years is associated with intestinal resection, although it proved to be more frequent in women (p<0.015), their conclusion was based on femoral hernias which presented greater percentage of resection (38.5%) compared to the inguinal (8%).

Regarding the type and side of the hernia, Akinci et al. [31], conducted a study in India to determine risk factors associated with unfavorable outcomes. A total of 685 patients with inguinal hernia who underwent emergency repair were evaluated, evidencing it to be more frequent in indirect hernias and on the right side, as corroborated in this study and in that of Pérez Lara et al. [32], although studies do not show significant differences.

On the other hand, intestinal obstruction and duration of incarceration in our investigation showed a higher frequency in the group with resection (p=0.007 and p=0.048 respectively). Like P. Chen et al. [33] and Ge et al. [34] shows significant values (p<0.001 and p=0.010, p=0.008 and p=0.062 respectively); who determined that the variables are risk factors for intestinal resection in inguinal hernias.

Developing predictors of intestinal resection from hematological systemic biomarkers turns out to be very useful. There are many investigations that have shown that PLR and NLR values are inflammatory predictors of cancer and effective as prognostics of survival, with NLR being the best prognostic indicator [35, 36].

In our investigation, the PLR showed higher values in those who presented resection in relation to those who did not (264.66±160.83 vs 161±56.78), demonstrating a statistically significant difference (p=0.010), unlike the red blood cell distribution width (RDW) that showed a mean of 44.07±3.72 vs 44.34±6.58, being insignificant. H. Köksal et al. [37], Turkey, included 102 patients undergoing emergency surgery for intestinal incarceration in hernias, comparing those who presented and did not present intestinal resection. Red blood cell distribution width (RDW), NLR and PLR were taken into account, showing that patients with intestinal resection presented higher NLR and PLR values in relation to the group without resection (p=0.019 and p=0.032, respectively); unlike RDW, which did not prove to be significant (p>0.05), however, in infectious pathologies of acute pancreatitis, necrotizing fasciitis and sepsis, it has been shown to be effective in predicting mortality (p<0.01) [38, 39, 40].

Particularly, Tanrıkulu et al. [41], Turkey, conducted a retrospective cohort study, evaluating the utility of NLR for early detection of patients diagnosed with acute mesenteric ischemia. It was shown that the NLR was significantly higher in the group with ischemia, compared to the group without ischemia (p<0.001), making early detection crucial to determine surgical management [42].

In a study conducted by H. Zhou et al. [43], in China, the value of neutrophil-to-lymphocyte ratio for the diagnosis of strangulated inguinal hernia was evaluated in 263 patients with inguinal hernias divided into 2 groups: 135 with intestinal ischemia and 128 without intestinal ischemia; determining NLR >6.5 as cut-off point and finding sensitivity of 75%, specificity of 68.9% and diagnostic accuracy of 72%. In our research, the same cut-off point was taken to relate the NLR as a predictor of intestinal resection; where 75% sensitivity was found, 93% specificity. Although Xie et al. [44], in 2017, identified that NLR ≥11.5 predicts the severity of incarcerated inguinal hernias, estimating sensitivity of 44% and specificity of 92%; although less sensitivity is appreciated, it proved to be a risk factor (OR=9.612, p=0.002).

In addition, in our analysis, it was determined with NLR >6.5: PPV, NPV, positive likelihood ratio (LR+) value and negative likelihood ratio (LR–) value, a result of 62.5%, 96.35%, 11.75 and 0.27, respectively. However, when analyzing the ROC curve, 5.14 was identified as the best cut-off point for NLR, a sensitivity, specificity, PPV, NPV, LR+ and LR– of 90%, 84.4%, 45%, 98.35%, 5.77 and 0.12, respectively, with an area under the curve of 0.92. This demonstrates that the cut-off point found has a higher diagnostic yield and good clinical utility, presenting LR+ values between 5—10 and LR– with a tendency to 0 [45].

In summary, early diagnosis and treatment are essential to prevent irreversible damage, with NLR >5.14 being a biomarker that predicts intestinal resection in incarcerated hernias. Some of the present limitations, due to its retrospective nature, are due to the fact that the patients were grouped according to the description in the records made in the hospital emergency room and findings of the operative report, and there may be errors.

Conclusion

The NLR proved to be a predictor of intestinal resection in incarcerated hernias, taking values greater than 5.4, with high diagnostic yield (sensitivity = 90%, specificity = 84.4%, positive predictive value = 45%, negative predictive value = 98.35%) and with good utility in clinical practice (LR+ =5.77 and LR– =0.12). On the other hand, the PLT/L index appears to be an independent biomarker that predicts the severity of patients with incarcerated hernias. It should be noted that the limitation of studies with biomarkers to predict the severity of incarcerated inguinal hernias invites more research to be carried out in order to corroborate the best cut-off point and its efficacy in clinical practice.

Authorship and contribution:

Viera C, Lozada J: conceptualization, formal analysis, research, methodology, resources, software, validation, visualization, writing.

Zavaleta C, Caballero J, Zafra C, Pozzuoli G: methodology, validation, proofreading and editing, conceptualization, formal analysis, writing.

Protection of people and animals: The authors declare that no experiments on humans or animals have been performed in this manuscript.

Data confidentiality: The authors declare that no patient data appears in this article.

Financing: None.

Conflicts of interest: None.

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INTRODUCTION

MATERIAL AND METHOD

RESULTS

CONCLUSIONS