Anabire 

et al. BMC Res Notes (2018) 11:353

https://doi.org/10.1186/s13104-018-3456-9 BMC Research Notes

RESEARCH NOTE Open Access

Hematological abnormalities in patients

with malaria and typhoid in Tamale Metropolis
of Ghana
Nsoh Godwin Anabire1, Paul Armah Aryee2 and Gideon Kofi Helegbe1*

Abstract 
Objective:  Anemia, Leukopenia, and thrombocytopenia are commonly observed hematological abnormalities
in malaria and typhoid patients. In this study, we evaluated the prevalence of cytopenias in patients with mono-
infections of plasmodium parasites (malaria group) or salmonella bacteria (typhoid group). Full blood counts from 79
patients (age ranging from 18 to 77 years) categorized into malaria and typhoid groups at the Tamale Central Hospital
were assessed.
Results:  Data generated were entered and analyzed using SPSS version 20 and Graphpad Prism 6. Values were
observed to be significant at p < 0.05. The prevalence of cytopenias were; 29.6, 48.0% for anemia, 38.9, 12.0% for
thrombocytopenia, 20.4, 12.0% for leukopenia, 13.0, 8.0% for bicytopenia and 5.6, 4.0% for pancytopenia in both
malaria and typhoid groups respectively. Between the two groups of patients, thrombocytopenia was significantly
associated with those in the malaria group (χ2 = 5.84, p < 0.016). No association was found between cytopenias and
gender in patients in the malaria group; however, the middle aged group, 36–55 years, was significantly associated
with anemia (χ2 = 12.97, p < 0.002). Cytopenias were not associated with gender, and with different age categories in
patients in the typhoid group.
Keywords:  Cytopenias, Malaria, Typhoid, Tamale metropolis

Introduction hemo-phagocytosis [13, 17]. Elsewhere, 94/61.3% ane-

Cytopenias are blood cell abnormalities that result from mia, 70/40% thrombocytopenia and 12/4% leukopenia
reduction in the major hematopoietic cell lines such as have been reported among adults with malaria or typhoid
red blood cells causing anemia, leukocytes causing leu- respectively [14, 18, 19].
kopenia and thrombocytes causing thrombocytopenia. Bicytopenia and pancytopenia usually result from
Bicytopenia occurs where there is a reduction below ref- direct or indirect decreasing effect on hematopoietic cell
erence ranges in any two of the major cell lines [1]. The production in the bone marrow [20–22]. These kinds of
simultaneous presence of anemia, thrombocytopenia and cytopenias are not uncommon in malaria; bone marrow
leukopenia in a person is termed pancytopenia. diagnosis of adults with bicytopenia and pancytopenia
Anemia [2–5], leukopenia [6–9] and thrombocyto- has shown that 3% of bicytopenia and 6% of pancytope-
penia [10–16] are commonly presented in plasmodium nia were caused by malaria [23, 24]. Even though bone
and salmonella infections. The occurrence of Cytope- marrow studies have shown no clear explanation for the
nias may be attributed to bone marrow suppression and peripheral blood pancytopenia in typhoid fever [25], a
case report of severe pancytopenia in an adult was attrib-
uted to hemo-phagocytosis [26].
*Correspondence: [email protected]
1
Despite many global studies reporting anemia, throm-
Department of Biochemistry & Molecular Medicine, School of Medicine
and Health Sciences, University for Development Studies, P. O. Box TL
bocytopenia and leukopenia with malaria and typhoid in
1883, Tamale, Ghana adults, limited studies of these cytopenias exist in Ghana.
Full list of author information is available at the end of the article The studies in Ghana, are mostly on anemia in children

© The Author(s) 2018. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License
(http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium,
provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license,
and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/
publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Anabire et al. BMC Res Notes (2018) 11:353 Page 2 of 6

[27–30] and in pregnant women [31–34]. Thus, this study manufacturer’s protocol. The presence of malaria para-
was intended to determine the prevalence and associa- sites was confirmed by microscopy using thick blood
tion of cytopenias in adults with plasmodium or salmo- smears which were stained with 20% Giemsa solution at
nella infections in Tamale. pH 7.2 [37]. The reading of the blood smears and inter-
pretation of the results were done as previously reported
Main text [38].
Methods The slide agglutination method previously described
Study area [39] was performed for typhoid using commercially avail-
The study was conducted in the Tamale metropolis; the able Widal kits (Lab Care Diagnostics, Mumbai, India,
Northern Regional capital of Ghana. The metropolis has Catalogue number: CW0111). Briefly, patients’ plasma
13% of the total land area of the Northern Region (70, was titrated in the following volumes 40, 20, 10 and 5 μl.
383 square km), and a total population of 223,252 com- One plate was designated for antigen-O and the other
prising 111,109 males and 112,143 females [35]. antigen-H. Later, one drop of antigen-O and antigen-H of
Salmonella typhi were added to patient’s plasma distrib-
Study design, study site and population uted on the respective plates. This was then mixed and
A hospital based cross-sectional study was conducted rocked and agglutination observed and interpreted as
from February to April 2015 on patients with mono- previously reported [39].
infections of plasmodium parasites or salmonella bac- Hb-Hemoglobin, WBC-White blood cell and PLT-
teria between the ages of 18–77  years at Tamale central Platelets were analyzed using the automated blood cell
Hospital. Tamale Central Hospital is one of the north- analyzer Sysmex XS-500i (Sysmex Corporation, Kobe,
ern regional hospitals and serves nearly 240,000 people Japan). Anaemia was diagnosed by Hb < 12 g/dl for non-
with numerous referrals from other districts in northern pregnant females and Hb < 13  g/dl for males [40], while
Ghana. PLT count <  150  ×  109/l and WBC count < 4.0  ×  109/l
were used respectively to determine thrombocytope-
Sample size and exclusion criteria nia and leukopenia [41]. Bicytopenia was determined
Sample size was obtained based on the number of adults if a subject had a combination of any 2 cytopenias and
that showed up with either malaria or typhoid within the pancytopenia as simultaneously having all three forms of
period of sampling. Pregnant women and individuals cytopenia.
diagnosed with helminthiasis, sickle cell disease, and kid-
ney disease were excluded from this study.
Statistical analysis
Data collection and processing Data were analyzed using SPSS Version 20 (IBM Corpo-
Demographic data (including sex and age) of each study ration, Chicago, USA) and Graphpad Prism 6 (GraphPad
participant was collected using a standardized question- Software Inc., San Diego, USA). All test statistics with p
naire (Additional file 1), after consent was obtained from values  <  0.05 were considered as statistically significant.
participants. Enumerators were given a one-day train- Continuous variables were described using median and
ing prior to data collection. The questionnaire was pre- interquartile range (IQR), and compared by Mann–Whit-
tested by random administration to 20 patients. Age was ney test, whilst categorical variables were presented as
categorized as follows: young adults (18–35), middle counts and percentages, and compared by Fisher’s exact
aged adults (36–55) and the aged (above 55) [36]. Clini- test or Pearson’s χ2 test.
cal diagnoses including sickle cell disease, kidney disease,
helminthiasis and urine pregnancy tests results were col-
lected from the patients’ folders by the clinicians on duty. Results
A Vacutainer K ­ 3EDTA tube (Anhui Kangning Indus- General characteristics of the study participants
trial group, Tianchang, China, Catologue Number: Out of the 79 individuals recruited for this study, major-
VG4000515) was used to collect 3  ml of venous blood ity, 55 (69.6%) were females (Table  1). The median age
from each participant for laboratory investigation. The was 31  years (IQR 21–47  years) with majority of the
blood samples were collected by a trained medical labo- study participants, 47 (59.5%) being young adults (18–
35  years), Table  1. The median hemoglobin count was
Malaria was diagnosed using CareStart™ HRP-2 rapid
ratory scientist.
12.8  g/dl (IQR 11.3–14.1  g/dl), whilst the median plate-
diagnostic test (Access Bio Inc., New Jersey, USA, Cata- let and white cell counts were 213 × 103/µL (IQR 142.0–
logue number: G0141). The testing, results reading and 287 × 103/µL) and 5.8 × 103/µL (IQR 4.5–7.0 × 103/µL)
interpretations were performed by strictly following the respectively.
Anabire et al. BMC Res Notes (2018) 11:353 Page 3 of 6

Table 1  Socio-demographic characteristics and hematological profile among malaria and typhoid patients

Characteristics Malaria group (N = 54) Typhoid group (N = 25) p value* (95% CI)

Age, years, median (IQR) 28 (20–45) 37 (24–54) 0.1544 (− 2.000 to 14.000)

Age category, years, n (%)
 18–35 36 (66.7) 11 (44.0) 0.069 (0.371 to 1.530)
 36–55 9 (16.7) 10 (40.0)
 56+ 9 (16.7) 4 (16.0)
Gender, n (%)
 Male 14 (25.9) 10 (40.0) 0.206 (0.192 to 1.435)
 Female 40 (74.1) 15 (60.0)
Hemoglobin, median (IQR) 13.3 (11.8–14.3) 12.6 (11.1–13.3) 0.0986 (− 1.800 to 0.200)
Platelets, median (IQR) 197.5 (120.5–273.5) 284.0 (175.5–320.0) 0.0065 (20.00 to 118.00)
White blood cells, median (IQR) 5.7 (4.3–6.6) 6.2 (4.9–9.8) 0.2301 (− 0.410 to 1.760)
Anemia, n (%) 16 (29.6) 12 (48.0) 0.112 (− 0.431 to 0.411)
Thrombocytopenia, n (%) 21 (38.9) 3 (12.0) 0.016 (1.241 to 17.550)
Leukopenia, n (%) 11 (20.4) 3 (12.0) 0.530 (0.474 to 7.430)
Bicytopenia, n (%) 7 (13.0) 2 (8.0) 0.711(0.392 to 8.911)
Pancytopenia, n (%) 3 (5.6) 1 (4.0) 1.000 (0.139 to 14.300)
Source: Field Survey. *Analyzed using Mann–Whitney test and Pearson’s χ2 test or Fisher’s exact test. Two tailed p value significant at p < 0.05
Malaria group patients with plasmodium mono-infection, Typhoid group patients with salmonella mono-infection

Prevalence and association of cytopenias in patients and leukopenia in patients presenting with malaria
with malaria or typhoid or typhoid at the health facilities, not much is known
The prevalence of cytopenias were; 29.6, 48.0% for ane- about the prevalence of these cytopenias among adults
mia, 38.9, 12.0% for thrombocytopenia, 20.4, 12.0% in Ghana; most especially in northern Ghana. Thus,
for leukopenia, 13.0, 8.0% for bicytopenia and 5.6, 4.0% providing the impetus for this study in Tamale. To
for pancytopenia in patients with mono-infections of the best of our knowledge, we are, for the first time,
plasmodium and salmonella respectively (Table  1). reporting the prevalence of cytopenias in patients with
While thrombocytopenia was significantly associated malaria or typhoid in Ghana.
(p < 0.016), with patients in the malaria group, anaemia, In the current study, thrombocytopenia was found to
leukopenia, bicytopenia and pancytopenia were inde- be the most prevalent in the adults with plasmodium
pendent of either groups (Table  1). Similar levels of Hb infection. This contradicts 2 studies [18, 19] that showed
and leucocytes were observed between both groups, anemia as the most prevalent cytopenia in malaria
however, levels of platelets were statistically lower, patients. However, both studies were conducted in south
p = 0.007 in the malaria group compared to the typhoid Asia where the dominant malaria parasite (P. vivax) is dif-
group (Table 1). Pancytopenia was only found in females ferent from that in Ghana (P. falciparum). Unlike P. vivax,
(7.5% in malaria and 6.7% in typhoid), Table  2. Cytope- P. falciparum is very virulent; it multiples rapidly in the
nias were observed to be independent of gender and blood and has the ability to sequester into diverse host
most age categories for either groups, however, the mid- organs [44]. It has been shown that some P. falciparum
dle aged malaria group, was significantly associated with infected-erythrocytes can bind platelets to form platelet-
anemia (p = 0.002), Table 2. mediated clumps [45] and postulations are that immune
mediated lysis of these clumps cause thrombocytopenia
in P. falciparum infection. Thus, differences in parasite
Discussion strains could be a possible reason for the difference seen
Malaria and typhoid are quite common in Tamale in this study; more so because [19] realized a significant
because the prevailing warm and humid climate is increase in the incidence of thrombocytopenia in P. fal-
conducive for the infection, concomitant with poor ciparum cases than in P. vivax cases. Our findings of a
sanitary practices that promote the infections [42]. higher prevalence and significant association of throm-
Malaria endemicity is nearly the same across the year bocytopenia with malaria adds to studies indicating that
but peaks slightly in the rainy season [43]. Despite thrombocytopenia is an indicator of malaria in the adult
the frequent diagnoses of anemia, thrombocytopenia population [46].
Anabire et al. BMC Res Notes (2018) 11:353 Page 4 of 6

Table 2  Association between cytopenias; and gender and age groups in malaria (N = 54) and typhoid patients (N = 25)
α β α β
Characteristics Malaria group Typhoid group Malaria group Typhoid group p value* (95% CI)

Anemia
Yes, n (%) No, n (%)
α
 Male 4 (28.6) 6 (60.0) 10 (71.4) 4 (40.0) 1.000 (0.244–3.574), β0.428 (0.439–11.530)
 Female 12 (30.0) 6 (40.0) 28 (70.0) 9 (60.0)
α
 18–35 6 (16.7) 6 (54.5) 30 (83.3) 5 (45.5) 0.002 (0.009–0.346), β0.798 (0.318–10.210)
 36–55 7 (77.8) 4 (40.0) 2 (22.2) 6 (60.0)
 56+ 3 (33.3) 2 (50.0) 6 (66.7) 2 (50.0)
Thrombocytopenia
Yes, n (%) No, n (%)
α
 Male 6 (42.9) 0 (0.0) 8 (57.1) 10 (100.0) 0.723 (0.363–4.308), β0.051 (0.003–1.409)
 Female 15 (37.5) 6 (40.0) 25 (62.5) 9 (60.0)
α
 18–35 14 (38.9) 3 (27.3) 22 (61.1) 8 (72.7) 0.349 (0.027–12.300), β0.114 (0.390–3.772)
 36–55 2 (22.2) 0 (0.0) 7 (77.8) 10 (100.0)
 56+ 5 (55.6) 0 (0.0) 4 (44.4) 4 (100.0)
Leukopenia
Yes, n (%) No, n (%)
α
 Male 2 (14.3) 1 (10.0) 12 (85.7) 9 (90.0) 0.708 (0.108–3.053), β0.179 (0.017–1.680)
 Female 9 (22.5) 6 (40.0) 31 (77.5) 9 (60.0)
α
 18–35 8 (22.2) 2 (18.2) 28 (77.8) 9 (81.8) 0.752 (0.248–21.110), β0.612 (0.153–3.360)
 36–55 2 (22.2) 1 (10.0) 7 (77.8) 9 (90.0)
 56+ 1 (11.1) 0 (0.0) 8 (88.9) 4 (100.0)
Bicytopenia
Yes, n (%) No, n (%)
α
 Male 3 (21.4) 1 (10.0) 11 (78.6) 9 (90.0) 0.358 (0.475–12.690), β1.000 (0.106–12.460)
 Female 4 (10.0) 1 (6.7) 36 (90.0) 14 (93.3)
α
 18–35 2 (5.6) 1 (9.1) 34 (94.4) 10 (90.9) 0.057 (0.016–0.860), β0.811(0.048–2.076)
 36–55 2 (22.2) 1 (10.0) 7 (77.8) 9 (90.0)
 56+ 3 (33.3) 0 (0.0) 6 (66.7) 4 (100.0)
Pancytopenia
Yes, n (%) No, n (%)
α
 Male 0 (0.0) 0 (0.0) 14 (100.0) 10 (100.0) 0.560 (0.018–7.611), β1.000 (0.017–12.460)
 Female 3 (7.5) 1 (6.7) 37 (92.5) 14 (93.3)
α
 18–35 2 (5.6) 1 (9.1) 34 (94.4) 10 (90.9) 0.589 (0.038–5.858), β0.811(0.048–2.076)
 36–55 1(11.1) 1 (10.0) 8 (88.9) 9 (90.0)
 56+ 0 (0.0) 0 (0.0) 9 (100.0) 4 (100.0)
Source: Field Survey. *Analyzed using Pearson’s χ2 test or Fisher’s exact test, αand βrepresent p values for association of cytopenias with gender and with age groups in
Malaria group: patients with plasmodium mono-infection, and Typhoid group: patients with salmonella mono-infection, respectively. Two tailed p value significant at
p < 0.05. 95% CI 95% confidence interval

While extensive studies have been conducted on middle aged group, 35–55 years but was, however, gen-
the occurrence of anemia in children and pregnant der independent. Even though it has been shown that
women with malaria [2–5], little is known of such stud- anemia in malaria patients differ in different ages [17],
ies in non-pregnant female and male adults. In areas it is not clear why anemia is significantly associated
with high malaria transmission, adults usually develop with this particular age group. Nevertheless, it is tempt-
semi-immunity to malaria due to exposure to several ing to speculate that immune reaction is very active in
different clones of malaria parasites. As such, adults this age group resulting in high loss of uninfected RBCs
are mostly asymptomatic, with low parasite loads that as well as the infected ones [47]. This should prompt a
could lead to anemia and its related complications. In closer look at anemia with malaria infection in this age
this study, anemia was strongly associated with the category in Tamale.
Anabire et al. BMC Res Notes (2018) 11:353 Page 5 of 6

Even though leukopenia was the least prevalent cyto- Limitation

penia, its prevalence was quite significant, and could This study was conducted within a relatively shorter
confound the estimation of malaria parasite density in period and the sample size was small. Since malaria
adults in Tamale based on the WHO criteria of WBC endemicity is nearly constant within the metropolis,
count of 8000 cells/μL. an all year investigation of these cytopenias in patients
The high prevalence of anemia recorded in the with malaria or typhoid would be important in substan-
adults with typhoid is similar to a study by [14]. This tiating the findings in this study.
finding could be attributed to myeloid maturation
arrest and decrease in the number of erythroblasts as Additional files
shown by [13]. The independence of the cytopenias
with typhoid, age and gender among the study popula- Additional file 1. Document used in the collection of socio-demographic
and health data. This is a blank document which contains the question-
tion may suggest that Hb, PLT and WBCs counts may naire used in the collection of socio-demographic characteristics, and the
not be good hematological markers for the diagnosis of health records of the study participants.
typhoid in adults in Tamale. Additional file 2. Data set of the subjects. This is a SPSS document con-
Pancytopenia and bicytopenia are a common hema- taining data transribed from the questionnaire.
tological problem encountered in clinical practice,
which have multiple causes and the underlying pathol-
ogy determines the management and prognosis of the Abbreviations
Hb: hemoglobin; WBCs: white blood cells; PLT: platelets; IQR: interquartile
patients. Bicytopenia and pancytopenia were observed range; RBCs: red blood cells; WHO: World Health Organization.
in both infections; and the knowledge that both cyto-
penias are seen in quite a number of malaria and Authors’ contributions
GKH and PAA conceived and designed the study. Questionnaire administra-
typhoid patients in Tamale is important information tion, laboratory analysis and data entering were performed by NGA. NGA, GKH
that would help in timely diagnosis and proper man- and PAA analyzed the data. NGA drafted the manuscript with GKH and PAA.
agement of such cases, leading to earlier discharge GKH supervised the study. All authors read and approved the final manuscript.
of the patient. Unlike many studies that had male Author details
dominance in pancytopenia cases [48–51], we real- 1
 Department of Biochemistry & Molecular Medicine, School of Medicine
ized that pancytopenia was only found in females for and Health Sciences, University for Development Studies, P. O. Box TL 1883,
Tamale, Ghana. 2 Department of Nutritional Sciences, School of Allied Health
either infection, which could possibly be attributed to Sciences, University for Development Studies, P. O. Box TL 1883, Tamale, Ghana.
the female dominance in this study. This falls in line
with what pertains in Ghana, where women are more Acknowledgements
We extend our heartfelt gratitude to the numerous clinicians at Tamale central
likely to access health care. More to the point, women Hospital for their enormous support. Again we thank the staff at registry
often have to ask for permission from their husbands and patients’ folders unit, and the staff at the hematology unit of the Tamale
in order to access treatment for themselves, which may Central Hospital for their immeasurable efforts. We also thank all our study
participants for their patience and agreeing to be part of this study.
delay depending on whether their husbands or family
elders would agree [52]. This may explain why in this Competing interests
study, the worse form of cytopenia, pancytopenia is The authors declare that they have no competing interests.
only found in females, because the longer it takes for Availability of data and materials
one to get an appropriate treatment for these infec- The datasets supporting the findings of this article are available in this manu-
tions, the more damage the disease causes to one’s script (Additional file 2).
hematopoietic system. Consent for publication
Not applicable.

Ethics approval and consent to participate

Conclusion Ethical approval for the study was obtained from the School of Medicine and
The high prevalence and association of thrombocy- Health Sciences (SMHS) and the School of Allied Health Sciences (SAHS) joint
topenia with malaria in adults in Tamale buttresses ethical review board of the University for Development Studies, Ghana. Writ-
ten informed consent was provided by each study participants.
numerous findings of low platelets count as a reliable
diagnostic marker for malaria in adult populations in Funding
Africa. The association of anemia with the middle aged Not applicable.
adults with malaria should prompt a closer look at ane-
mia with plasmodium infection in this age category in Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in pub-
Tamale. Our finding of pancytopenia in only females, lished maps and institutional affiliations.
should prompt strengthening of education on barriers
preventing females from accessing healthcare delivery.
Anabire et al. BMC Res Notes (2018) 11:353 Page 6 of 6

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