ORIGINAL�ARTICLE

ABSTRACT
Objective: To determine the frequencies of different types of granulomas in patients suffering from cutaneous 
leishmaniasis.
 Study Design: Descriptive cross-sectional study.
Place and Duration of Study: Armed Forces Institute of Pathology, Combined Military Hospital, Rawalpindi, Dec 
2021 to Oct 2022.
Materials and Methods: This study was conducted on 290 patients suffering from cutaneous leishmaniasis. 
Patients aged between 18 and 70 years of both genders were included, while those who had already received 
treatment for leishmaniasis, or suffered from mucocutaneous or visceral leishmaniasis were excluded. All 
patients underwent a punch biopsy, tissue which was stained with hematoxylin and eosin, and then studied for 
the presence of granulomas and Parasitic Index. PCR was done to confirm species of Leishmania causing 
disease. Data was analyzed using SPSS 26.0.
Results: Our study population had a median age of 38.00 (16 - 63) years, with a male majority: 185 (63.8%). 
Granuloma formation was seen in 185 (63.8%) patients: 121 (41.7%) had a tuberculoid granuloma and 13 
(4.5%) had suppurative granulomas, while 51 (17.6%) had caseating ones. L. Tropica was the most seen 
organism accounting for 255 (87.9%) cases, L. Major was the infective organism in 26 (9.0%) patients, while L. 
Infantum was found in 9 (3.1%) cases. Factors such as gender (p=0.273), age of the patient (p=0.901), disease 
duration (p=0.366), site of lesion (p=0.669), type of skin lesion (p=0.490), parasite index (p=0.297) and species 
of Leishmania (p=0.870) did not have any significant association with the development of non-caseating 
granulomas.
Conclusion: Chronic granulomatous inflammation is  a common finding on histopathology in cutaneous 
leishmaniasis and vigilance is required to avoid confusion with other endemic granulomatous skin conditions.

Key Words: Cutaneous Leishmaniasis, Mycobacterium Tuberculosis, Non Caseating Granulomas, Polymerase 
Chain Reaction, Ridley Modified Parasitic Index.

with just the cutaneous form having an estimated 
1,2 

incidence of one million new cases per annum.
Pakistan accounts for approximately 10% of the 
global disease burden for all forms of leishmaniasis 

3 
which amounts to an estimated half a million cases.
Leishmania is diagnosed using a wide variety of tests 
such as direct visualization of the parasite in a tissue 
specimen, skin hypersensitivity testing, antibody 
detection and molecular methods such as 
polymerase chain reaction, however, such definitive 
but expensive methods are not readily available in 
resource-poor countries, and diagnosis is based on 

4,5
clinical and tissue examination.
However, this diagnostic approach is not without 
risk: Leishmania is known for its ability to imitate 
different skin conditions not only macroscopically, 

6 
but microscopically as well. Histologically, the 
disease may present in wide variety of ways including 

Introduction
Leishmaniasis is a common tropical disorder 
attributed to an obligate intracellular protozoan 
which is transmitted to humans by the bite of the 
Phlebotomus or Lutzomyia sand-fly and causes 
manifestations by which it is classified into the 
cutaneous, mucocutaneous, and visceral disease, 

Non-Caseating Granulomas in Skin Biopsies of Leishmania Cases
1 2 3 4 5 

Siyab Ahmad , Nadeem Zafar , Muhammad Owais Qurni , Shabir Ahmad Orakzai , Muhammad Atif Khalil , Wajahat Ahmad 
6

Khan

Correspondence:
Dr. Siyab Ahmad
Department of Histopathology
Armed Forces Institute of Pathology, Rawalpindi
E-mail: siyabamc@gmail.com

1,2,5,6
Department of Histopathology

Armed Forces Institute of Pathology, Rawalpindi
Department of Histopathology 
3
Combined Military Hospital, Multan

4
Department of Pathology

Swat Medical College, Swat

Received: November 19, 2022; Revised: January 10, 2023
Accepted: January 31, 2023

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15https://doi.org/10.57234/jiimc.march23.1574



parasitized macrophages with lymphocy tic 
7 

infiltration or non-specific chronic inflammation. It is 
also associated with the formation of granulomas: 
these can vary from non-specific ill-defined 

7,8 
granulomas to epithelioid  granulomas. Cases of 
cutaneous leishmaniasis have been demonstrated to 
show caseous necrosis as well, and have the 

9
potential to be misdiagnosed as tuberculosis,  or 
may be mischaracterized as a non-infectious disease 

10
such as pyoderma gangrenosum.  We conducted 
this study with the aim of determining frequencies of 
different types of granulomatous inflammation in 
patients suffering from cutaneous leishmaniasis. 
Understanding the nature of the myriad types of 
histological pictures that leishmaniasis can present 
with is an important concept to understand, the lack 
of which can result in the misdiagnosis of the 
disease, and the institution of inappropriate 
management, with potentially dire consequences 
for the patient and the treating team. Recognition 
that leishmaniasis can mimic the histological picture 
of other diseases and remaining sentient to the 
possibility of the presence of this endemic parasite 
will go a long way towards reducing the morbidity 
associated with it. 

Materials and Methods
We conducted this descriptive cross-sectional study 

st st
between 1  Dec 2021 and 31  Oct 2022 in Armed 
Forces Institute of Pathology, Combined Military 
Hospital, Rawalpindi, on 290 patients suffering from 
cutaneous leishmaniasis, after obtaining informed 
consent. Approval from the institutional review 
board of the hospital was obtained. Sample selection 
was carried out via non-probability, consecutive 
sampling. The WHO sample size calculator was used 
to calculate the sample size keeping a confidence 
level of (1-α) of 95%, an absolute precision (d) of 0.05 
and an anticipated population proportion (P) of 
0.748, which was the percentage of patients with 
cutaneous leishmaniasis suffering from non-

11
caseating granulomas, from Aoun et al. . For 
convenient sampling patients aged between 15 and 
70 years of both genders were included in the study. 
Patients who had received previous treatment for 
leishmaniasis, or suffered from mucocutaneous or 
visceral leishmaniasis, or those who were suffering 
from malignancies, immunosuppressed states, drugs 
that caused immunosuppression, or patients who 

had a positive PCR for Mycobacterium Tuberculosis 
were excluded.
All patients' details were documented for 
demographic data such as age and gender on 
enrollment, as well as for duration of disease, site of 
lesion and type of skin eruption. Each patient 
underwent a punch biopsy of about 5 mm, which was 
processed and preserved as tissue blocks.  
Subsequent slides were prepared using hematoxylin 
and eosin stain. At this point, patients were 
documented for type of granuloma, if any.  Diagnosis 
of leishmaniasis as well as confirmation of species 
was done by Polymerase Chain Reaction (PCR) 
targeting kinetoplast DNA. 
 In a brief, the formalin-fixed, paraffin-embedded 
tissue blocks were used to extract DNA. Leishmania 
ribosomal internal transcribed spacer 1 (ITS1) was 
amplified using primers. This was done in a 50 mL 
amplification reaction. The following stages and 
conditions were employed for amplification on the 
Px2 thermal cycler: 95 C for 2 min, 35 cycles of (95 C 
for 20 sec, 53 C for 30 sec, 72 C for 1 min), and 72 C for 

11 
6 min.
Furthermore, Ridley modified parasitic index 
quantifies the parasitic load of amastigotes in 
cutaneous lesions and has a numerical score from 1 

 11
to 6 as displayed in table I.

Table I : Ridley Modified Parasitic Index

Data was analyzed using the Statistical Package for 
the Social Sciences (IBM SPSS Statistics for Windows 
version 26, IBM Corp; Armonk, USA). Mean and 
standard deviation was calculated for quantitative 
variables specifically patient age and duration of 
disease. Qualitative variables like gender, site of skin 
lesion, type of eruption, Parasitic Index, species of 
Leishmania, presence and type of granuloma were 
recorded in terms of frequency and percentage. 
Patients were divided into three groups: one with 
caseating granulomas, one without and one with no 

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granuloma formation. Quantitative variables were 
compared across groups using the independent 
samples t-test / One-Way ANOVA test while the Chi 
square test / Fischer exact test was used for 
qualitative variables and a p-value of ≤ 0.05 was 
considered significant.

Results
This study was conducted on a total of 290 patients 
with a median age of 38.00 (16 - 63) years. Most of 
the patients were male i.e., 185 (63.8%), while the 
median duration from onset of skin lesion to 
presentation was 27.00 (6 - 49) weeks. A total of 112 
(38.6%) had a lesion present on the upper limbs, the 
lower limbs were affected in 89 (30.7%), while the 
head and neck region and the trunk were involved in 
80 (27.6%) and 9 (3.1%) cases, respectively. Nodules 
were seen in 159 (54.8%) i.e., most of our cases, 
followed by ulcers: 97 (33.4%) and 34 (11.7%) had 
papular lesions at presentation.
Table-II shows the patient characteristics distributed 
according to gender at the time of presentation. 

(87.9%) cases, while Leishmania Major (L. Major) 
was the infective organism in 26 (9.0%) patients, 
while Leishmania Infantum (L. Infantum) were found 
in the least number of patients i.e., 9 (3.1%). 
Granuloma formation was seen in 185 (63.8%) 
patients: 121 (41.7%) had a tuberculoid granuloma 
while 51 (17.6%) and 13 (4.5%) had caseating and 
suppurative granulomas, respectively. Thus, a total 
of 134 (46.2%) patients had non-caseating 
granulomas while and 105 (36.2%) had no evidence 
of any granuloma on histology.

Table II: Patients Characteristics According to Gender

Table-III displays the histological characteristics of 
the leishmaniasis for the sample according to gender.  
A Parasite Index of One was seen in 27 (9.3%) 
patients, cases with an index of Two were 45 (15.5%), 
those with a Parasite Index of Three accounted for 59 
(20.3%) cases, while an index of Four, Five and Six 
were seen in 67 (23.1%), 63 (21.7%), and 29 (10.0%) 
cases, respectively. Leishmania Tropica (L. Tropica) 
was the most seen organism accounting for 255 

Table III: Histological Characteristics According to Gender

Table-IV shows the comparison between patients 
with non-caseating granulomas, those without and 
those patients who did not have granulomas. Factors 
such as gender, age of the patient, disease duration, 
site of lesion, type of skin lesion, parasite index and 
species of Leishmania were not associated with the 
development of non-caseating granulomas.

Discussion
Granuloma formation occurs in response to 
persistent inflammatory stimulation which results in 
the aggregation of inflammatory cells (primarily 
macrophages): an immune protective mechanism 
which neutralizes foreign/pathogenic matter by 

12
encapsulation and neutralization.  Cutaneous 
leishmaniasis, in its limited form, is usually cleared 
spontaneously by the immune system without 

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Table IV: Comparison of Different Variables with and 
Without Chronic Granulomatous Inflammation

caseating, 17.6% caseating), while 36.2% did not 
appear to have any granulomas on histological 
examination in our study. Most of the non-caseating 
granulomas were tuberculoid, while a minority were 
suppurative. Cardozo et al reported that 84.0% of 
their cases had granuloma formation, with the 
majority of these having non-caseating granulomas, 

15 
while less than 1.0% had caseating ones. Most of 
their patients had ill-defined histiocytic aggregates 
rather than the well-formed granulomas seen in our 

15 
study. Aoun et al reported granuloma formation in 
61.5% of their study, of which 46.1% were non-

11 
caseating, while 15.4% demonstrated caseation,  
while Andrade-Narvaez et reported that 43.8% had 
granulomas in their study, none of whom 

16 
demonstrated caseation. The variability in results 
may be attributable to a number of reasons: 
granuloma formation may be dependent on a 
number of host and disease factors which were not 
homogenous across the studies mentioned above, 
which may account for the differences in histological 
patterns seen.
Our study had a median age of 38.00 (16 - 63) years, 
age did not appear to have any association with the 
visualization of non-caseating granulomas, 
(p=0.901). This figure is in keeping with existing 
studies on the subject such as Debash et al who 
reported that the maximum number of cases of 
cutaneous leishmaniasis were seen in the range of 15 
to 49 years in their study, while Bisetegn et al 
reported a mean age of 31.9 ± 14.29 years for their 

17,18 
sample. Moreover, Aoun et al also  reported that 
there was no association between the development 

11
of different types of granulomas and age.
The most of our study sample was male i.e., 185 
(63.8%). Gender did not appear to have an 
association with the formation of non-caseating 
granulomas, (p=0.273). Wijesinghe et al and 
Solomon et al both noted that cutaneous 
leishmaniasis was more likely to be present in males, 
which is likely due to increase outdoor activities and 
differences in clothing when compared to 

19,20
females.  In addition, Aoun et al also concluded 
that gender did not appear to be associated with the 

11
development and type of granuloma.
Most patients i.e., 38.6% had a lesion on the upper 
limbs, while the lower limbs had lesions in 30.7% 
cases. The head and neck region were affected in 

intervention in about a month, however, that is not 
always necessarily the case and the disease may take 
as long as six years to clear, necessitating 
confirmation of diagnosis and institution of 

13
appropriate treatment.  However, the process of 
diagnosis may be difficult in areas without molecular 
methods of disease confirmation i.e., reliant on 
histology for establishing presence of the disease: 
cutaneous leishmaniasis is known as the great 
imitator and it has the ability to mimic almost any 

14
dermatosis, hence the requirement for this study.
Granulomas were seen in 63.8% (46.2% non-

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27.6% patients while the trunk was least affected: 
3.1% cases, in our study. Anatomical location of the 
lesion did not appear to have an association with the 
development of non-caseating granulomas, 
(p=0.669). Rather et al noted in their study that 
lesions tended to occur on exposed areas, while 
Aoun et al also confirmed that the bites were most 
commonly found on the extremities and the head 
and neck region as in our study, and that location did 
not have any effect on the development of non-
caseating granulomas, a fact that was also concurred 

11,22
with by Aguado et al.
The principle macroscopic skin manifestation of 
disease were nodules in our study which accounted 
for 54.8% cases. Ulcers were seen in 33.4% patients 
while papular lesions were the least common and 
occurred in 11.7%. The type of macroscopic skin 
lesion did not appear to have a significant association 
with the development of non-caseating granulomas, 
(p=0.490). Our results were in contrast to Wijesinghe 
et al who noted that the occurrence of papules, 
nodules and ulcers occurred at the roughly same 
f re q u e n c i e s  o f  3 4 . 7 % ,  3 2 . 7 %  a n d  3 0 . 6 % ,  

19 
respectively, while Aoun et al reported that the 
majority of patients had nodular lesions (49.2%), 
while ulcerative lesions were also common (49.2%), 

11 
which was in agreement with our results. Variability 
in results between our study and Wijesinghe may be 
due to the delayed presentation seen in the latter 
study which may lead to worsening of the skin lesion. 
Aoun et al, like our study, also noted that the type of 
macroscopic lesion was not associated with the 

11
development of non-caseating granulomas.  
The Parasitic Index did not appear to have a 
relationship with the development of non-caseating 
granulomas, (p=0.297), in our study, which was 

11 
concurred with by Aoun et al (p=0.09), however, 
Wijesinghe et al reported that having a higher 
Parasitic Index was associated with a higher risk of 
developing granulomas, (p=0.027), which was at 

19 
odds with our study. This aspect of research 
requires further study before concrete conclusions 
can be drawn, but studies have shown that the 
number of organisms reduce as the cutaneous 
leishmaniasis becomes chronic but the granulomas 

23
form regardless.
Lastly, L. Tropica was the most seen species in our 
study, accounting for 87.9% of our sample, followed 

by L. Major, which affected 9.0% patients, while L. 
Infantum was isolated in 3.1% cases. None of the 
s p e c i e s  h a d  a ny  p ro p e n s i t y  t o w a r d s  t h e  
development of non-caseating granulomas, 
(p=0.870). Previous studies have shown the most 
common organism in Pakistan is L.Tropica in patients 
with cutaneous leishmaniasis which forms the bulk 
of cases, while L. Major accounts for a minor 

24 
percentage, and L. Infantum is rarely seen. Studies 
have also previously demonstrated that no species is 
associated with the development of non-caseating 

11
granulomas.  

Study Limitations
This research protocol was conducted as a single-
center study and was limited by its small sample size. 
Secondly, this study was performed on military 
personnel and their wards which has robust 
screening programs which may have resulted in early 
detection of disease which may or may not have 
affected the frequency of granuloma formation. 
Lastly, a case-control study would give a better idea 
of the association of different disease and patient 
factors with the formation of different types of 
granulomas and should be the subject of future 
research.

Conclusion
C u t a n e o u s  L e i s h m a n i a s i s  i s  a  c o m m o n l y  
encountered disease that may present as a 
diagnostic dilemma in our part of the world due to its 
ability to mimic other common skin conditions such 
as tuberculosis and leprosy in terms of histological 
features. Recognition that the disease can commonly 
cause manifestations such as non-caseating and 
caseating granulomas, the pathologist must remain 
vigilant in making the correct diagnosis and institute 
appropriate and timely management. Future 
research should focus on the effect of granuloma 
formation on response to treatment and prognosis in 
terms of scarring.

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CONFLICT OF INTEREST
Authors declared no conflicts of Interest.

GRANT SUPPORT AND FINANCIAL DISCLOSURE
Authors have declared no specific grant for this 
research from any funding agency in public, 
commercial or nonprofit sector.

DATA SHARING STATMENT
The data that support the findings of this study 
are available from the corresponding author 
upon request.

This is an Open Access article distributed under the terms of the Creative Commons Attribution- Non-
Commercial 2.0 Generic License.

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