The Use of Biochemical Markers in Complicated and Uncomplicated Acute Diverticulitis
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Int Surg 2021;105:380–388
DOI: 10.9738/INTSURG-D-16-00241.1
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The Use of Biochemical Markers in
Complicated and Uncomplicated Acute
Diverticulitis
Dulitha Kumarasinghe1, Assad Zahid2, Greg O’Grady3, Timothy YQ Leow4, Tabrez
Sheriff5, Grahame Ctercteko6, Martijn Gosselink7, Sanjay Adusumilli8
1
School of Medicine, University of Western Sydney, Blacktown Hospital Campus, Blacktown, Sydney,
Australia
2
Westmead Hospital Colorectal Research Fellow, Westmead, Sydney, Australia
3
Auckland Hospital, Auckland, Grafton, New Zealand
4
School of Medicine, University of Western Sydney, Blacktown Hospital Campus, Blacktown, Sydney,
Australia
5
School of Medicine, Bond University, Gold Coast, Australia
6
Department of Colorectal Surgery, Westmead Hospital, Sydney, Australia
7
Department of Colorectal Surgery, Westmead Hospital, Sydney, Australia
8
Department of Surgery, Blacktown Hospital, Sydney, Australia
Objective: Diverticulosis is extremely common in western society. A recent study has
shown that outpatient, nonantibiotic management of acute uncomplicated diverticulitis
may be a feasible and safe option. However, the ability to identify these patients is still
difficult. This study explores the ability of white cell count, C-reactive protein, and bilirubin
in differentiating patients with complicated and uncomplicated diverticulitis, as well as
progression to surgical intervention.
Methods: This is a retrospective study of patients admitted with acute diverticulitis over a
5-year period (2009–2014) at a single institution in Australia. Patients were classified into 3
Corresponding author: Assad Zahid, BSc(Med) MBBS MS MPhil FRACS, 72 Hobart Place, Illawong, NSW 2234, Australia.
Tel.: þ61 41 329 5984; E-mail: assadzahid@hotmail.com
380 Int Surg 2021;105MARKERS OF ACUTE DIVERTICULITIS KUMARASINGHE
groups; uncomplicated diverticulitis, complicated diverticulitis without surgery, and
complicated diverticulitis with surgery. Analysis of variance (ANOVA) and Bonferroni’s
post hoc analyses were used to compare markers across the groups.
Results: A total of 541 patients met the inclusion criteria for this study. One-way ANOVA
showed a significant difference in white cell count (P , 0.0001), C-reactive protein (P ,
0.0001), and bilirubin (P ¼ 0.0006) between all 3 groups. Post hoc analyses showed a
significant difference in white cell count, C-reactive protein, and bilirubin when comparing
uncomplicated diverticulitis against complicated diverticulitis without surgery (P , 0.05)
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and complicated diverticulitis with surgery (P , 0.05). White cell count also showed a
significant difference when comparing complicated diverticulitis without surgery and
complicated diverticulitis with surgery (P , 0.05).
Conclusions: White cell count, C-reactive protein, and bilirubin can distinguish between
uncomplicated and complicated diverticulitis.
Key words: Diverticulitis – CRP – Inflammatory markers
D iverticulosis is an extremely common disease
in western society, mainly affecting people
over the age of 40.1,2 Although many will remain
positive predictive value for perforation in acute
diverticulitis and may be a focus for future
research.18
asymptomatic, 10%–25% of individuals with diver- Although most studies have indicated trends for
ticulosis will eventually develop symptomatic di- WCC and CRP to be higher in complicated
verticulitis. Of these, 15%–20% will develop diverticulitis, specific values to be used with
significant complications,3 which include abscess, diagnostic reliability have varied widely. A recent
perforation, fistula formation, and bowel obstruc- study has shown that outpatient, nonantibiotic
tion and may require more invasive forms of management of acute uncomplicated diverticulitis
treatment.4–6 The mainstay of treatment for uncom- may be a feasible and safe option.22 However, the
plicated diverticulitis is conservative including ability to identify these patients is still difficult.
monitoring, antibiotics, and analgesia, whereas Bilirubin, WBC, and CRP are commonly measured
patients with complicated diverticulitis may need as part of a standard workup for abdominal pain in
more invasive procedures such as percutaneous the emergency department. This study has been
drainage or surgery.7
undertaken with a view to clarifying the value of
The clinical diagnosis of acute diverticulitis is
inflammatory markers to differentiate between
often straightforward, but to differentiate between
uncomplicated and complicated diverticulitis.
uncomplicated and complicated will require further
imaging.8–10 Computed tomography (CT) scanning
therefore has a central role in the diagnosis of Methods
suspected cases with a sensitivity of 94% and Study design and setting
specificity of 99%.11–13
Many researchers have investigated the efficacy This retrospective cohort study was performed at a
of biochemical inflammatory markers in the diag- single teaching hospital in Western Sydney, Austra-
nosis of acute diverticulitis.14–16 Leukocytosis has lia, was approved by the local institutional review
been demonstrated to be more prevalent in severe committee, and meets the guidelines of the respon-
cases of diverticulitis,16 with white cell count (WBC) sible governmental agency. The electronic medical
shown to be significantly higher in complicated records (EMRs) of patients who were admitted with
versus uncomplicated diverticulitis.15,17,18 Similarly, acute diverticulitis between January 2009 and
C-reactive protein (CRP) has been shown as a useful December 2014 were retrospectively reviewed. The
supporting tool in diagnosing the clinical severity of patients with CT-confirmed diagnosis were further
acute diverticulitis.14,18–21 Among other markers, looked at to ascertain whether there was a signifi-
hyperbilirubinemia, although having a low sensi- cant relationship with biochemical markers (WCC,
tivity, has been shown to have a high specificity and CRP, and bilirubin) and the severity of diverticulitis.
Int Surg 2021;105 381KUMARASINGHE MARKERS OF ACUTE DIVERTICULITIS
Table 1 Demographic data for 541 patients with acute diverticulitis
Uncomplicated Complicated Complicated Complicated
diverticulitis: diverticulitis; diverticulitis diverticulitis
All patients Hinchey Ia Hinchey Ib, II, without surgery with surgery
Demographics (n ¼ 541) (n ¼ 374) III, IV (n ¼ 167) (n ¼ 131) (n ¼ 36)
Mean age at 55.33 (14.15) 56.17 (13.9) 53.46 (14.59) 53.15 (14.32) 54.58 (15.66)
presentation (SD), y
Sex
Male (%) 279 (51.6) 183 (48.9) 96 (57.5) 72 (55) 24 (66.7)
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Female (%) 262 (48.4) 191 (51.1) 71 (42.5) 59 (45) 12 (33.3)
Data collection across the groups. The sensitivities, specificities, and
postive and negative predictive values were calcu-
A diagnosis-specific code was used to identify
lated at differrent thresholds to assess their diag-
patients admitted with acute diverticulitis from the
nostic capability.
Emergency Department (ED). This is the principal
form of contact of such patients to our institution.
All patients underwent a standard diagnostic Results
workup in ED of biochemical markers, including a
full blood count, electrolytes, liver enzymes and A total of 797 patients were identified for screening
bilirubin, and CRP. The demographics (age and sex) for inclusion in the study, due to a diagnostic coding
and specific laboratory values (bilirubin, WBC, CRP) for diverticulitis. Of these, 256 were subsequently
at initial presentation to ED were collected from excluded because they did not meet criteria for
patient EMRs. CT and operation reports for each severity stratification, either because they lacked
admission were reviewed to verify the diagnosis of definitive confirmation of diverticulitis by CT or
diverticulitis and stratify patients into uncomplicat- operation report.
ed diverticulitis (Hinchey Ia) or complicated diver- An analysis was performed on the remaining 541
ticulitis (Hinchey Ib, II, III, IV) using the modified patients. Of these patients, 374 (69.1%) had uncom-
Hinchey classification.6,23 Patients who did not have plicated diverticulitis, whereas 167 (30.9%) had
a CT scan on presentation were not included as the complicated diverticulitis. Of the 167 patients who
diagnosis could not be verified. Patients were then had complicated diverticulitis, 131 (24.2% of total,
further classified into 3 subgroups, including un- 78.4% of complicated cases) had no surgical inter-
complicated diverticulitis (UC), complicated diver- vention, whereas 36 (6.7% of total, 21.6% of
ticulitis without surgery (C-NS), and complicated complicated cases) had some form of surgical
diverticulitis with surgery (C-S), reflecting the intervention. Demographic data according to sever-
management they received. ity stratification are depicted in Table 1.
Indicators for surgical interventions included
severe or diffuse peritonitis, uncontained perfora- Use of WBC as a marker
tion, large radiologically undrainable abscesses, and
failure of conservative treatment. To date, all One-way ANOVA showed that WBC was signifi-
patients who present to our institution with a cantly different between UC, C-NS, and C-S groups
diagnosis of diverticulitis undergo admission and (P , 0.0001). Post hoc analyses showed a statistically
receive antibiotics treatment as a mainstay. significant elevation in WBC when comparing UC
versus C-NS (mean difference [MD] ¼ 2.340; 95%
confidence interval [CI]: 3.422, 1.258; P , 0.05),
Analyses
UC versus C-S (MD ¼5.410; 95% CI: 7.270, 3.550;
All data were analyzed by Prism version 6.0 by P , 0.05), and C-NS versus C-S (MD ¼ 3.070; 95%
Graphpad Software (La Jolla, California). Descrip- CI: 5.075, 1.065; P , 0.05). A receiver operator
tive statistics and 1-way analysis of variance curve (ROC) demonstrates the significance of the
(ANOVA) were conducted to compare WBC, CRP, comparison of WBC between the uncomplicated
and bilirubin between UC, C-NS, C-S groups. Post and complicated with surgery groups (Fig. 1).
hoc analyses using Bonferroni’s multiple compari- Supplemental Table 2 shows that patients with a
sons test were then used to identify relationships WBC higher than 15 3 109 mg/L had a positive
382 Int Surg 2021;105MARKERS OF ACUTE DIVERTICULITIS KUMARASINGHE
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Fig. 1 ROC curve of WBC between uncomplicated and Fig. 2 ROC curve of CRP between uncomplicated and
complicated with surgery. Area under the curve, 0.719. complicated diverticulitis. Area under the curve, 0.701.
predictive value of 57% for having complicated C-S groups (P ¼ 0.0006). Post hoc analyses using
diverticulitis, which increased to 86% at a WBC Bonferroni’s multiple comparisons test showed a
higher than 19 3 109 mg/L. statistically significant elevation in bilirubin when
comparing UC versus C-NS (MD ¼ 2.543; 95% CI:
Use of CRP as a marker 0.6345, 4.452; P , 0.05) and UC versus C-S (MD ¼
One-way ANOVA analysis showed that CRP was 3.757; 95% CI: 6.971, 0.5433; P , 0.05). However,
significantly different between UC, C-NS, and C-S there was no significant difference in bilirubin
groups (P , 0.0001). Post hoc analyses showed a elevation when comparing C-NS and C-S (MD ¼
statistically significant elevation in CRP when 1.214; 95% CI: 4.616, 2.188; P . 0.05). An ROC
comparing UC and C-NS (MD ¼ 57.54; 95% CI: curve of bilirubin between uncomplicated and
76.30, 38.77; P , 0.05) and UC versus C-S (MD ¼ complicated diverticulitis groups is shown in Fig.
89.44; 95% CI: 121.00, 57.92; P , 0.05). However, 3. Supplemental Table 2 shows that patients with a
there was no significant difference in CRP elevation bilirubin higher than 20 lmol/L had a positive
when comparing C-NS and C-S (MD ¼ 31.90; 95% predictive value of 52% for having complicated
CI: 65.91, 2.12; P . 0.05). A comparison of CRP diverticulitis.
between groups is illustrated in Fig. 2 in the form of
a ROC curve with the area under the curve being Combining bilirubin, WCC, and CRP
0.701. Supplemental Table 2 shows that patients
Supplemental Table 2 shows sensitivities, specifici-
with a CRP higher than 100 mg/L had a positive
ties, positive predictive values, and negative pre-
predictive value of 59% for having complicated
diverticulitis, which increased to 71% at a CRP dictive values at different thresholds for bilirubin,
higher than 200 mg/L. A CRP more than 5 mg/L WBC, and CRP. Patients with a bilirubin greater
had a negative predictive value of 91%. than 20 lmol/L, WBC greater than 15 3 109 mg/L,
and CRP greater than 100 mg/L had a positive
predictive value of 92% for having complicated
Use of bilirubin as a marker
diverticulitis. This increased to 100% with a biliru-
One-way ANOVA analysis showed that bilirubin bin greater than 20 lmol/L, WBC greater than 17 3
was significantly different between UC, C-NS, and 109 mg/L, and a CRP greater than 200 mg/L.
Int Surg 2021;105 383KUMARASINGHE MARKERS OF ACUTE DIVERTICULITIS
Males versus females
Incidentally, 96 of 167 (57.5%) patients in the
complicated diverticulitis group and 24 of 36
(66.7%) patients in the complicated diverticulitis
with surgery group were male. Chi-square analysis
showed no significant difference in sex between UC,
C-NS, and C-S (P ¼ 0.08), as well as uncomplicated
versus complicated diverticulitis (P ¼ 0.07).
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Discussion
Biochemical inflammatory markers are routinely
used to support the clinical diagnoses of acute
diverticulitis. Studies have shown that certain
elevated inflammatory markers may have potential
use in differentiating between complicated and
uncomplicated cases; however, their exact role is
yet to be defined.14–21 Table 2 demonstrates recent
studies that have been conducted and the findings
of significance for the biochemical marker tested.
Statistical analysis of our large cohort of patients
in this study showed that WBC, CRP, and bilirubin
Fig. 3 ROC curve of bilirubin between uncomplicated and
were significantly elevated when comparing un-
complicated diverticulitis. Area under the curve, 0.608.
complicated diverticulitis to complicated diverticu-
litis, both with and without surgery. However, only
WBC was significantly elevated when comparing
complicated diverticulitis with surgery and compli-
cated diverticulitis without surgery.
Fig. 4 Scatter graph of WCC results with number of patients in each group.
384 Int Surg 2021;105MARKERS OF ACUTE DIVERTICULITIS KUMARASINGHE
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Fig. 5 Scatter graph of CRP results with number of patients in each group.
WBC is considered one of the most important remarkable that it is elevated in diverticulitis as
markers of inflammation in acute diverticulitis. Past shown in past studies.14,15,18,20 This study found a
studies have also shown WBC to be higher in statistically significant difference between the CRPs
complicated diverticulitis15,17,18 but have shown to of uncomplicated and complicated diverticulitis
have lower sensitivities and specificities than with and without surgical intervention. Although
CRP.18–24 However, the study of Van de Wall et al the highest values of CRP tended to be from cases of
evaluating 426 patients showed that, although the diverticulitis that would eventually need surgical
mean WBC was generally higher in complicated
diverticulitis, it had poor diagnostic value in Table 2 Significance of biochemical markers with diagnosis of
diverticultis
discriminating between the two.15 Longstreth et al
looked at WCC and noted that a result of greater No. CRP
than 11,000/mm3 was significant for differentiating Author Year patients WBC mg/L Bilirubin
between nondiagnositc/moderate diverticulitis and
Makela et al 2016 200 NS
severe (P , 0.0001).25 Figure 4 demonstrates a Makela et al 2015 350 .150
scatter graph of the WCC results and a line Kechagias et al 2014 182 .170
highlighting the significant value of Longstreth et (Makela)
Nizri et al 2014 295 .90
al. Wide variation of results above and below this
Van de Wal et al 2012 426 NS .175
line are seen with regard to both complicated and Longstreth et al 2012 741 Sign
uncomplicated patients. Kaser et al 2010 247 NS 200 NS
CRP has become a routine test in the emergency Tursi et al 2008 50 Sign Sign
department and has been the focus of many studies John et al 2007 100 NS Sign
in the past. As an acute phase reactant, it is not NS, not significant; Sign, significant
Int Surg 2021;105 385KUMARASINGHE MARKERS OF ACUTE DIVERTICULITIS
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Fig. 6 Scatter graph of bilirubin results with number of patients in each group.
intervention, no significant difference was found significant difference in bilirubin levels between
between the CRP values of surgical and nonsurgical uncomplicated and complicated disease.
intervention in complicated diverticulitis. Interest- It is of interest that the observed series in this study
ingly, Makela et al demonstrated in their retrospec- showed an incidental finding that most patients in the
tive review that a CRP of .149.5 mg/L significantly complicated diverticulitis with surgery group were
discriminated between acute uncomplicated diver- male. Although not statistically significant (P ¼ 0.07),
ticulits from complicated diverticultis.14 Figure 5 males trended toward being more likely to have
demonstrates a scatter diagram of the CRP results complicated disease than females.
from our study, and a line is placed highlighting the When used alone, all 3 markers did not have
signficant value of Makela et al. What can be seen sufficiently high positive predictive values to deter-
here is that there is significant variation of individ- mine complicated diverticulitis. The highest value
ual patient results with both complicated and was obtained with a WCC greater than 19 3 109 mg/
uncomplicated disease. L showing a positive predictive value of 86%.
Bilirubin, on the other hand, is a marker that has However, when all 3 markers are used in combina-
had very little investigation in relation to acute tion, these numbers dramatically rise as should be
diverticulitis, although it has been shown to have expected. In this cohort, all patients with a bilirubin
high sensitivities and specificities for perforation in greater than 20 lmol/L, WBC greater than 17 3
acute sigmoid diverticulitis.18 Hyperbilirubinemia 109mg/L, and CRP greater than 200 mg/L had
has been described in case reports of complicated complicated diverticulitis.
acute diverticulitis.26,27 and has been linked to Of particular interest was the scatter of the results
extrahepatic bacterial infection inducing cholestasis of patients presenting with uncomplicated and
and hepatic portal vein gas as a cause.27,28 Our complicated diverticulitis (Figs. 4–6). Wide variation
study extends these observations by showing a of results is noted for patients in the uncomplicated
386 Int Surg 2021;105MARKERS OF ACUTE DIVERTICULITIS KUMARASINGHE
and complicated groups making diagnosis based 10. Laurell H, Hansson LE, Gunnarsson U. Acute diverticulitis–
purely on biochemical makers very difficult. Despite clinical presentation and differential diagnostics. Colorectal Dis
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