Fatma Yilmaz1,
Bugra Saglam2, Ufuk Gorduk1, Ugur Kalan1,
Hacer Berna Afacan Ozturk1, Ahmet Kursad Gunes1
and Murat Albayrak1.
1 Etlik City
Hospital, Department of Hematology, Ankara, Turkey.
2 Medicalpoint Hospital, Department of Hematology,
Gaziantep, Turkey.
Correspondence to:
Fatma Yilmaz. Etlik City Hospital, Department of Hematology,
Yenimahalle, 06170, Ankara, Turkey. Tel.: 0506 882 3869. E-mail:
dr.fatmak@hotmail.com
Published: September 01, 2024
Received: April 26, 2024
Accepted: August 17, 2024
Mediterr J Hematol Infect Dis 2024, 16(1): e2024071 DOI
10.4084/MJHID.2024.071
This is an Open Access article distributed
under the terms of the Creative Commons Attribution License
(https://creativecommons.org/licenses/by-nc/4.0),
which permits unrestricted use, distribution, and reproduction in any
medium, provided the original work is properly cited.
|
Abstract
Background: Patients with leukaemia
are exposed to infections as long as they are neutropenic. During this
period, anorectal pathologies are among the common foci of infection
with high mortality. In this study, we aim to investigate the factors
that may have a predictive effect on early diagnosis and rapid
intervention in perianal complications occurring in neutropenic
patients diagnosed with leukaemia.
Methods: A total of 90 patients with acute leukaemia, including
45 patients with anorectal pathology and 45 patients without anorectal
pathology, were analysed. Demographics, blood group, BMI, haemogram and
biochemical parameters at the time of diagnosis, and types of perianal
pathology were recorded.
Results: In the group of patients with anorectal pathology,
WBC, lymphocytes, monocytes, and LDH were significantly (p<0.05)
higher, and platelets, MPV, and PCT were significantly (p<0.05)
lower. The multivariate model showed significant-independent
(p<0.05) efficacy of WBC and MPV values in differentiating patients
with and without anorectal pathology. A significant efficacy was
observed at the WBC cut-off of 17000 [area under the curve 0.656
(0.542-0.770)] and the MPV cut-off of 10 [area under the curve 0.667
(0.554-0.780)] in differentiating patients with and without anorectal
pathology.
Conclusion: Anorectal pathologies are common foci of infection
in patients with acute leukaemia. Having predictive parameters that may
help for early intervention will help the clinician. This is the first
study in the literature to compare a control group with a group with
anorectal pathologies in leukaemia patients providing a cut-off for WBC.
|
Introduction
Acute leukaemia is
diagnosed with a blast rate of ≥20% in the bone marrow. Leukemias,
which are characterised by abnormal leukocyte production, are
categorised into subgroups based on proliferation rate, source cell and
genotypic characteristics.[1] Patients with leukaemia
are exposed to infections as long as they are neutropenic. During this
period, anorectal pathologies are among the common foci of infection.
Although the diagnosis is difficult, the diagnosis can be made based on
the findings from physical examination and imaging modalities. Although
symptoms may be masked in immunosuppressed patients, they are usually
accompanied by complaints such as pain, swelling and constipation,
which may progress to systemic infection.[2] A wide
spectrum of conditions can be encountered, ranging from mild lesions to
more severe conditions such as abscesses, and has a high mortality rate
of 11-57% in patients with neutropenia.[3] Early
recognition of anorectal pathologies and rapid intervention in
neutropenic patients are among the factors that will significantly
affect mortality.
In this study, we aim to investigate the factors that may have a
predictive effect on early diagnosis and rapid intervention in perianal
complications occurring in the neutropenic period in patients with
leukaemia receiving cytotoxic chemotherapy.
Materials and Methods
Materials and
Methods. Patients
with newly diagnosed leukaemia who received induction cytotoxic
chemotherapy in the Haematology Department between June 2022 and
October 2023 were retrospectively analysed. Patients were questioned
about their complaints daily during the neutropenia period, and routine
physical examinations, including perianal examinations, were performed
and recorded in their files. Perianal MRI was performed on patients
with suspicious complaints (anal pain, difficulty sitting, fever) or
physical examination findings (anal tenderness, redness, discharge)
during the febrile neutropenia period. Patients diagnosed with
haemorrhoids, abscesses, fistula and fissures by perianal MRI were
included in the 'patient with perianal pathology' group. The 'patients
without perianal pathology' group included patients who were newly
diagnosed with leukaemia and received induction therapy and who had no
perianal complaints or findings during the neutropenia period (the
focus of infection was not in the perianal region). Patients with a
history of perianal pathology or surgery before the diagnosis of
leukaemia and those with a diagnosis of diabetes mellitus were excluded
from the study. A total of 90 patients, including 45 patients with
perianal pathology and 45 patients without perianal pathology, were
enrolled in the study. Demographics, blood group, BMI (body mass
index), haemogram and biochemical parameters at the time of diagnosis,
and types of perianal pathology were recorded. The types of perianal
pathology of the patients were classified according to the Perianal MRI
results.
Statistical
Analysis. Mean, standard deviation, median, minimum, maximum
value frequency and percentage were used for descriptive statistics.
The distribution of variables was checked with the Kolmogorov-Smirnov
test. Independent Samples t-test and Mann-Whitney U test were used to
compare the quantitative data. A chi-square test was used to compare
the qualitative data. Univariate and multivariate logistic regression
was used to show the effect level. ROC analysis was used to show the
effect level. SPSS 27.0 was used for statistical analyses.
Ethical
Approval and Informed Consent. All procedures performed in
studies involving human participants were in accordance with the
ethical standards of the institutional and/or national research
committee and with the 1964 Helsinki Declaration and its later
amendments or comparable ethical standards. The study was approved by
the Ethics Committee of Etlik City Hospital, Ankara, Turkey
(AEŞH-EK1-2023-179).
Results
The study in which 90
patients, including 45 patients with anorectal pathology and 45 control
group, were analysed consisted of 42 (46.7%) men and 48 (53.3%) women.
The mean age of the patients included in the study was 44.9±15.0 years,
and 66 (73.3%) were receiving treatment for AML (Acute Myeloid
Leukaemia) and 24 (26.7%) for ALL (Acute Lymphoblastic Leukaemia). The
distribution of age, gender and diagnosis did not differ significantly
(p>0.05) between the groups with and without anorectal pathology. In
our study, 20 patients (22.2%) were diagnosed with haemorrhoids, 10
(11.1%) with abscess, 10 (11.1%) with fistula and 5 (5.6%) with
fissure. BMI was 25.8±4.5 and 26.4±6.2, respectively, in the groups
with and without anorectal pathology, and no statistically significant
difference was found between the two groups. Demographics and other
general characteristics of the patients are analysed in detail in Table 1. In the group without
anorectal pathology, WBC (White Blood Cell) was 23.5±40.2, lymphocyte
count was 4.7±6.3, monocyte count was 10.6±22, LDH (Lactate
Dehydrogenase) was 753.1±1107, while in the group with anorectal
pathology WBC was 50.7±66.3, lymphocyte count 21.8± 47.7, monocyte
count 24.3± 34.8, LDH 790.1±629.2 and these values were statistically
significantly (p<0.05) higher in the group with anorectal pathology.
Haemoglobin, PDW (Platelet Distribution Width), neutrophil, glucose,
urea, creatinine, ALT (Alanine Aminotransferase), AST (Aspartate
Aminotransferase), albumin, vitamin B12, folate, ferritin levels did
not differ significantly (p>0.05) between the groups. Platelets were
52.3± 66.4, MPV (Mean Platelet Volume) 9.8± 1.3, PCT (Plateletcrit)
0.05± 0.06 in the group with anorectal pathology and were significantly
(p<0.05) lower than the group without anorectal pathology (Table 2).
![Table 1](https://www.mjhid.org/mjhid/article/download/5711/version/2814/4575/46094/Table%201.jpg) |
- Table 1.
Descriptive statistics of the data and distribution of demographic
parameters of the patients.
|
![Table 2](https://www.mjhid.org/mjhid/article/download/5711/version/2814/4575/46095/Table%202.jpg) |
- Table 2.
Comparison of group parameters with and without anorectal pathology.
|
The parameters in Table 2 were evaluated with the
appropriate method (Independent Sample t-test (t) / Mann-Whitney U test
(m) / Chi-square test (X2)), and univariate regression analysis was
performed on the parameters that were found to be statistically
significant (p <0.05). The univariate model showed significant
(p<0.05) activity of WBC, MPV, lymphocyte, and monocyte in
differentiating patients with and without anorectal pathology. WBC,
MPV, lymphocyte and monocyte parameters that showed statistically
significant effect in distinguishing patients with and without
anorectal pathology in the univariate model were analysed by
multivariate regression. The multivariate model showed
significant-independent (p<0.05) efficacy of WBC and MPV values in
differentiating patients with and without anorectal pathology (Table 3, Figure 3 and 4).
![Table 3](https://www.mjhid.org/mjhid/article/download/5711/version/2814/4575/46096/Table%203.jpg) |
- Table 3.
Univariate and Multivariate Model.
|
![Figure 3 and 4](https://www.mjhid.org/mjhid/article/download/5711/version/2814/4575/46081/Figure%203%20and%204.jpg) |
- Figure 3 and 4.
WBC and MPV values.
|
A significant cut-off for
differentiation of intergroup patients was 17000 [area under the curve
0.656 (0.542-0.770)] for WBC and 10 [area under the curve 0.667
(0.554-0.780)] for MPV. The sensitivity, positive predictive rate,
specificity, specificity and negative predictive rate were 66.7%,
65.2%, 64.4% and 65.9%, respectively, for the intergroup
differentiation of patients at the WBC cut off of 17000 (Table 4, Figure 1).
![Table 4](https://www.mjhid.org/mjhid/article/download/5711/version/2814/4575/46097/Table%204.jpg) |
- Table 4. For WBC,
cut off.
|
![Figure 1](https://www.mjhid.org/mjhid/article/download/5711/version/2814/4575/46079/Figure%201.jpg) |
- Figure 1. White
Blood Cell.
|
The sensitivity, positive
predictive rate, specificity, specificity and negative predictive rate
were 60.0%, 69.2%, 73.3% and 64.7%, respectively, for the intergroup
differentiation of patients at the MPV cut off of 10 (Table 5, Figure 2).
![Table 5](https://www.mjhid.org/mjhid/article/download/5711/version/2814/4575/46098/Table%205.jpg) |
- Table 5. MPV cut
off.
|
![Figure 2](https://www.mjhid.org/mjhid/article/download/5711/version/2814/4575/46080/Figure%202.jpg) |
- Figure 2.
|
Discussion
There are many factors
affecting clinical susceptibility, especially for infections in
patients with haematological malignancies. Factors affecting the risk
of infection can generally be analysed into three main groups:
disease-related, patient-related, and treatment-related.[4]
Factors associated with the disease include neutropenia, impaired
granulocyte function,[5] the potential of immature
myeloid cells to inhibit the antigen-specific T-cell response,[6] and immunoglobulin deficiency due to dysregulation of
the humoral immune system.6 Patient-related factors include age,
malnutrition and low baseline BMI. Both T and B cell functions
deteriorate with age, and the function of the immune system decreases.
Prolonged neutropenia with high-dose chemotherapy[7]
may result in mucositis and impaired gastrointestinal flora after
broad-spectrum antibiotic use.[8]
Pneumonia, skin and soft tissue infections, anorectal pathologies,
urinary tract infections, mucositis, neutropenic enterocolitis, and
catheter infections can be listed as possible foci of infection that
may occur during neutropenia in haematological malignancies.[9]
In patients with haematological malignancies, anal and perianal
pathologies are among the common complications with the contribution of
mucosal damage during neutropenia, and infections are the most common
cause.[10] In this patient population, diagnosis of
anorectal pathologies may be difficult, but the diagnosis can be made
based on redness, swelling, tenderness, fluctuation and imaging
findings on physical examination.[3] The incidence was
7.3% in a study by Büyükaşık Y et al., [11]
5.8% in a study by Greval et al.,[12] and 6.7% in a
study by Chen C et al.[2] In neutropenic process,
perianal infections tend to recur in every cycle.[2]
These infections are observed in a wide spectrum from mild lesions,
e.g. local cellulitis and haemorrhoids, to more severe conditions, e.g.
abscesses and are associated with a mortality rate of 11-57% in
patients with neutropenia.[3] In addition to the
serious mortality risk, they cause severe anal pain, discomfort, and
management difficulties in the course of treatment.[13]
In the study by Perazzoli et al., anorectal pathologies were observed
as abscesses in 27%, anal fissures in 23% and haemorrhoids in 19%.14 In
our study, haemorrhoids were reported in 22.2% (20), abscesses in 11.1%
(10), fistulas in 11.1% (10) and fissures in 5.6% (5).
The study included 42 (46.7%) men and 48 (53.3%) women. The mean age of
the patients included in the study was 44.9±15.0 years, and 66 (73.3%)
were receiving treatment for AML and 24 (26.7%) for ALL. No significant
(p>0.05) difference was found between the groups with and without
anorectal pathology according to age, gender, diagnosis distribution
and BMI. In some studies in the literature, abscesses were more
frequent in patients diagnosed with AML than in patients diagnosed with
ALL.[2,10] In contrast, in other
literature studies, no correlation was found between the diagnosis and
the development of anal abscess.[11,15]
In the study by Chang H et al., the group with perianal abscess was
younger than the group without perianal abscess.[16]
In our study, WBC, lymphocyte, monocyte and LDH were significantly
(p<0.05) higher in the group with anorectal pathologies, while
platelets, MPV and PCT were significantly (p<0.05) lower in the
group without anorectal pathologies.
In a study by Orhan B et al., the prognosis was found to be worse, and
the need for the operation was higher in patients with anorectal
pathology with elevated WBC.[10]
A high monocyte count at the time of diagnosis was considered a poor
prognostic factor for overall survival.[17,18] In our
study, the presence of leucocytosis in the group with anorectal
pathology and the associated lymphocytosis and monocytosis can be
considered consistent with the literature.
Platelet count at the time of diagnosis varies in AML patients. Higher
leukocyte and blast counts were observed in the group with low platelet
count at the time of diagnosis (<20,000/109/L) compared to the group
with moderately high and very high platelet counts.[19]
Thus, the association of thrombocytopenia with elevated WBC is a
finding also observed in our study and is consistent with this
literature data.
Survival was higher in AML patients with a platelet count between
50,000 and 120,000 at the time of diagnosis compared to patients with
low or high platelet counts.[20] In our study,
platelet count was lower in the group with anorectal pathology. In
other words, low platelet count at the time of diagnosis is associated
with more frequent anorectal pathology and higher mortality.
The blood level of LDH increases with cell damage and tends to increase
as the severity of infection increases. Studies in the literature show
that LDH level has prognostic significance for infection.[21,22]
In our study, LDH level was also found to be higher in patients with
anorectal pathology. Elevated LDH is parallel with the occurrence of
anorectal pathology.
MPV and PCT are platelet parameters that are automatically calculated
in whole blood tests. MPV is one of the main platelet parameters, which
also reflects the proliferation, metabolism, platelet enzymatic
activity, and functional status of megakaryocytes. MPV can be used as a
reference to evaluate platelet production and function and to determine
the cause of thrombocytopenia.[23,24]
Studies have shown that a decrease in myeloproliferative function leads
to a decrease in platelets, while MPV decreases or remains unchanged.[25] In a 2014 study, Vinholt et al. suggested that
bleeding symptoms in patients with thrombocytopenia may be due to a
decrease in MPV.[26]
The literature contains studies demonstrating the relationship between
PCT and infection severity.[27,28] PCT was lower in
the group with anorectal pathology compared to the group without
anorectal pathology.
The univariate model showed significant (p<0.05) activity of WBC,
MPV, lymphocyte, and monocyte in differentiating patients with and
without anorectal pathology, whereas no significant (p>0.05)
activity of platelet, PCT, and LDH was observed (Table 4).
The multivariate model showed significant-independent (p<0.05)
efficacy of WBC and MPV values in differentiating patients with and
without anorectal pathology (Table 4).
A significant cut-off for differentiation of intergroup patients was
17000 [area under the curve 0.656 (0.542-0.770)] for WBC and 10 [area
under the curve 0.667 (0.554-0.780)] for MPV. The sensitivity, positive
predictive rate, specificity, specificity, and negative predictive rate
were 66.7%, 65.2%, 64.4% and 65.9%, respectively, for the intergroup
differentiation of patients at the WBC cut-off of 17000 (Table 4, Figure 1).
The sensitivity, positive predictive rate, specificity, specificity and
negative predictive rate were 60.0%, 69.2%, 73.3% and 64.7%,
respectively, for the intergroup differentiation of patients at the MPV
cut off of 10 (Table 5, Figure 2).
Conclusions
Anorectal pathologies are
common foci of infection in patients with acute leukaemia. Early
intervention is an important factor that will affect the patient’s
survival in the neutropenic period. Having predictive parameters that
may help for early intervention will help the clinician. Setting a
cut-off for WBC and MPV can be a serious guide. Multicentre studies
with a larger number of patients are needed to set a standard for these
cut-off values. In the literature, this study is the first to compare a
control group with a group of patients with anorectal pathologies in
leukaemia patients and to provide a cut-off for WBC and MPV, which were
considered significant independent variables in the multivariate model.
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