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Hematological abnormalities in patients with malaria and typhoid in Tamale Metropolis of Ghana

Hematological abnormalities in patients with malaria and typhoid in Tamale Metropolis of Ghana 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 (χ = 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 (χ = 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 has shown that 3% of bicytopenia and 6% of pancytope Anemia [2–5], leukopenia [6–9] and thrombocyto- - 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: ghelegbe@uds.edu.gh Despite many global studies reporting anemia, throm- Department of Biochemistry & Molecular Medicine, School of Medicine bocytopenia and leukopenia with malaria and typhoid in and Health Sciences, University for Development Studies, P. O. Box TL adults, limited studies of these cytopenias exist in Ghana. 1883, Tamale, 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 [38]. Main text The slide agglutination method previously described Methods [39] was performed for typhoid using commercially avail- Study area able Widal kits (Lab Care Diagnostics, Mumbai, India, The study was conducted in the Tamale metropolis; the Catalogue number: CW0111). Briefly, patients’ plasma Northern Regional capital of Ghana. The metropolis has was titrated in the following volumes 40, 20, 10 and 5 μl. 13% of the total land area of the Northern Region (70, One plate was designated for antigen-O and the other 383 square km), and a total population of 223,252 com- antigen-H. Later, one drop of antigen-O and antigen-H of prising 111,109 males and 112,143 females [35]. Salmonella typhi were added to patient’s plasma distrib- uted on the respective plates. This was then mixed and Study design, study site and population rocked and agglutination observed and interpreted as A hospital based cross-sectional study was conducted previously reported [39]. from February to April 2015 on patients with mono- Hb-Hemoglobin, WBC-White blood cell and PLT- infections of plasmodium parasites or salmonella bac- Platelets were analyzed using the automated blood cell teria between the ages of 18–77  years at Tamale central analyzer Sysmex XS-500i (Sysmex Corporation, Kobe, Hospital. Tamale Central Hospital is one of the north- Japan). Anaemia was diagnosed by Hb < 12 g/dl for non- ern regional hospitals and serves nearly 240,000 people pregnant females and Hb < 13  g/dl for males [40], while with numerous referrals from other districts in northern 9 9 PLT count <  150  ×  10 /l and WBC count < 4.0  ×  10 /l Ghana. were used respectively to determine thrombocytope- nia and leukopenia [41]. Bicytopenia was determined Sample size and exclusion criteria if a subject had a combination of any 2 cytopenias and Sample size was obtained based on the number of adults pancytopenia as simultaneously having all three forms of that showed up with either malaria or typhoid within the cytopenia. period of sampling. Pregnant women and individuals diagnosed with helminthiasis, sickle cell disease, and kid- ney disease were excluded from this study. Statistical analysis Data were analyzed using SPSS Version 20 (IBM Corpo- Data collection and processing ration, Chicago, USA) and Graphpad Prism 6 (GraphPad Demographic data (including sex and age) of each study Software Inc., San Diego, USA). All test statistics with p participant was collected using a standardized question- values  <  0.05 were considered as statistically significant. naire (Additional file  1), after consent was obtained from Continuous variables were described using median and participants. Enumerators were given a one-day train- interquartile range (IQR), and compared by Mann–Whit- ing prior to data collection. The questionnaire was pre- ney test, whilst categorical variables were presented as tested by random administration to 20 patients. Age was counts and percentages, and compared by Fisher’s exact categorized as follows: young adults (18–35), middle test or Pearson’s χ test. aged adults (36–55) and the aged (above 55) [36]. Clini- cal diagnoses including sickle cell disease, kidney disease, helminthiasis and urine pregnancy tests results were col- Results lected from the patients’ folders by the clinicians on duty. General characteristics of the study participants A Vacutainer K EDTA tube (Anhui Kangning Indus- Out of the 79 individuals recruited for this study, major- trial group, Tianchang, China, Catologue Number: ity, 55 (69.6%) were females (Table  1). The median age VG4000515) was used to collect 3  ml of venous blood was 31  years (IQR 21–47  years) with majority of the from each participant for laboratory investigation. The study participants, 47 (59.5%) being young adults (18– blood samples were collected by a trained medical labo- 35  years), Table  1. The median hemoglobin count was ratory scientist. 12.8  g/dl (IQR 11.3–14.1  g/dl), whilst the median plate- Malaria was diagnosed using CareStart HRP-2 rapid let and white cell counts were 213 × 10 /µL (IQR 142.0– diagnostic test (Access Bio Inc., New Jersey, USA, Cata- 3 3 3 287 × 10 /µL) and 5.8 × 10 /µL (IQR 4.5–7.0 × 10 /µL) logue number: G0141). The testing, results reading and respectively. interpretations were performed by strictly following the 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 χ 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 strains could be a possible reason for the difference seen Discussion in this study; more so because [19] realized a significant Malaria and typhoid are quite common in Tamale increase in the incidence of thrombocytopenia in P. fal- because the prevailing warm and humid climate is ciparum cases than in P. vivax cases. Our findings of a conducive for the infection, concomitant with poor higher prevalence and significant association of throm - sanitary practices that promote the infections [42]. bocytopenia with malaria adds to studies indicating that Malaria endemicity is nearly the same across the year 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 β Male 4 (28.6) 6 (60.0) 10 (71.4) 4 (40.0) 1.000 (0.244–3.574), 0.428 (0.439–11.530) Female 12 (30.0) 6 (40.0) 28 (70.0) 9 (60.0) α β 18–35 6 (16.7) 6 (54.5) 30 (83.3) 5 (45.5) 0.002 (0.009–0.346), 0.798 (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 β Male 6 (42.9) 0 (0.0) 8 (57.1) 10 (100.0) 0.723 (0.363–4.308), 0.051 (0.003–1.409) Female 15 (37.5) 6 (40.0) 25 (62.5) 9 (60.0) α β 18–35 14 (38.9) 3 (27.3) 22 (61.1) 8 (72.7) 0.349 (0.027–12.300), 0.114 (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 β Male 2 (14.3) 1 (10.0) 12 (85.7) 9 (90.0) 0.708 (0.108–3.053), 0.179 (0.017–1.680) Female 9 (22.5) 6 (40.0) 31 (77.5) 9 (60.0) α β 18–35 8 (22.2) 2 (18.2) 28 (77.8) 9 (81.8) 0.752 (0.248–21.110), 0.612 (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 β Male 3 (21.4) 1 (10.0) 11 (78.6) 9 (90.0) 0.358 (0.475–12.690), 1.000 (0.106–12.460) Female 4 (10.0) 1 (6.7) 36 (90.0) 14 (93.3) α β 18–35 2 (5.6) 1 (9.1) 34 (94.4) 10 (90.9) 0.057 (0.016–0.860), 0.811(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 β Male 0 (0.0) 0 (0.0) 14 (100.0) 10 (100.0) 0.560 (0.018–7.611), 1.000 (0.017–12.460) Female 3 (7.5) 1 (6.7) 37 (92.5) 14 (93.3) α β 18–35 2 (5.6) 1 (9.1) 34 (94.4) 10 (90.9) 0.589 (0.038–5.858), 0.811(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) 2 α β Source: Field Survey. *Analyzed using Pearson’s χ test or Fisher’s exact test, and represent 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 Additional files arrest and decrease in the number of erythroblasts as shown by [13]. The independence of the cytopenias Additional file 1. Document used in the collection of socio-demographic with typhoid, age and gender among the study popula- 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- taining data transribed from the questionnaire. Pancytopenia and bicytopenia are a common hema- tological problem encountered in clinical practice, which have multiple causes and the underlying pathol- Abbreviations ogy determines the management and prognosis of the 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- Authors’ contributions penias are seen in quite a number of malaria and 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. GKH supervised the study. All authors read and approved the final manuscript. agement of such cases, leading to earlier discharge of the patient. Unlike many studies that had male Author details dominance in pancytopenia cases [48–51], we real- Department of Biochemistry & Molecular Medicine, School of Medicine and Health Sciences, University for Development Studies, P. O. Box TL 1883, ized that pancytopenia was only found in females for Tamale, Ghana. 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 Acknowledgements with what pertains in Ghana, where women are more 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 Central Hospital for their immeasurable efforts. We also thank all our study in order to access treatment for themselves, which may 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 The authors declare that they have no competing interests. study, the worse form of cytopenia, pancytopenia is 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- script (Additional file 2). tions, the more damage the disease causes to one’s 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 ethical review board of the University for Development Studies, Ghana. Writ- topenia with malaria in adults in Tamale buttresses 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 Not applicable. Africa. The association of anemia with the middle aged adults with malaria should prompt a closer look at ane- Publisher’s Note mia with plasmodium infection in this age category in Springer Nature remains neutral with regard to jurisdictional claims in pub- Tamale. 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Hematological abnormalities in patients with malaria and typhoid in Tamale Metropolis of Ghana

Anabire, Nsoh; Aryee, Paul; Helegbe, Gideon
BMC Research Notes , Volume 11 (1) – Jun 5, 2018
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Springer Journals
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Copyright © 2018 by The Author(s)
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Biomedicine; Biomedicine, general; Medicine/Public Health, general; Life Sciences, general
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1756-0500
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10.1186/s13104-018-3456-9
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29871667
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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 (χ = 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 (χ = 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 has shown that 3% of bicytopenia and 6% of pancytope Anemia [2–5], leukopenia [6–9] and thrombocyto- - 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: ghelegbe@uds.edu.gh Despite many global studies reporting anemia, throm- Department of Biochemistry & Molecular Medicine, School of Medicine bocytopenia and leukopenia with malaria and typhoid in and Health Sciences, University for Development Studies, P. O. Box TL adults, limited studies of these cytopenias exist in Ghana. 1883, Tamale, 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 [38]. Main text The slide agglutination method previously described Methods [39] was performed for typhoid using commercially avail- Study area able Widal kits (Lab Care Diagnostics, Mumbai, India, The study was conducted in the Tamale metropolis; the Catalogue number: CW0111). Briefly, patients’ plasma Northern Regional capital of Ghana. The metropolis has was titrated in the following volumes 40, 20, 10 and 5 μl. 13% of the total land area of the Northern Region (70, One plate was designated for antigen-O and the other 383 square km), and a total population of 223,252 com- antigen-H. Later, one drop of antigen-O and antigen-H of prising 111,109 males and 112,143 females [35]. Salmonella typhi were added to patient’s plasma distrib- uted on the respective plates. This was then mixed and Study design, study site and population rocked and agglutination observed and interpreted as A hospital based cross-sectional study was conducted previously reported [39]. from February to April 2015 on patients with mono- Hb-Hemoglobin, WBC-White blood cell and PLT- infections of plasmodium parasites or salmonella bac- Platelets were analyzed using the automated blood cell teria between the ages of 18–77  years at Tamale central analyzer Sysmex XS-500i (Sysmex Corporation, Kobe, Hospital. Tamale Central Hospital is one of the north- Japan). Anaemia was diagnosed by Hb < 12 g/dl for non- ern regional hospitals and serves nearly 240,000 people pregnant females and Hb < 13  g/dl for males [40], while with numerous referrals from other districts in northern 9 9 PLT count <  150  ×  10 /l and WBC count < 4.0  ×  10 /l Ghana. were used respectively to determine thrombocytope- nia and leukopenia [41]. Bicytopenia was determined Sample size and exclusion criteria if a subject had a combination of any 2 cytopenias and Sample size was obtained based on the number of adults pancytopenia as simultaneously having all three forms of that showed up with either malaria or typhoid within the cytopenia. period of sampling. Pregnant women and individuals diagnosed with helminthiasis, sickle cell disease, and kid- ney disease were excluded from this study. Statistical analysis Data were analyzed using SPSS Version 20 (IBM Corpo- Data collection and processing ration, Chicago, USA) and Graphpad Prism 6 (GraphPad Demographic data (including sex and age) of each study Software Inc., San Diego, USA). All test statistics with p participant was collected using a standardized question- values  <  0.05 were considered as statistically significant. naire (Additional file  1), after consent was obtained from Continuous variables were described using median and participants. Enumerators were given a one-day train- interquartile range (IQR), and compared by Mann–Whit- ing prior to data collection. The questionnaire was pre- ney test, whilst categorical variables were presented as tested by random administration to 20 patients. Age was counts and percentages, and compared by Fisher’s exact categorized as follows: young adults (18–35), middle test or Pearson’s χ test. aged adults (36–55) and the aged (above 55) [36]. Clini- cal diagnoses including sickle cell disease, kidney disease, helminthiasis and urine pregnancy tests results were col- Results lected from the patients’ folders by the clinicians on duty. General characteristics of the study participants A Vacutainer K EDTA tube (Anhui Kangning Indus- Out of the 79 individuals recruited for this study, major- trial group, Tianchang, China, Catologue Number: ity, 55 (69.6%) were females (Table  1). The median age VG4000515) was used to collect 3  ml of venous blood was 31  years (IQR 21–47  years) with majority of the from each participant for laboratory investigation. The study participants, 47 (59.5%) being young adults (18– blood samples were collected by a trained medical labo- 35  years), Table  1. The median hemoglobin count was ratory scientist. 12.8  g/dl (IQR 11.3–14.1  g/dl), whilst the median plate- Malaria was diagnosed using CareStart HRP-2 rapid let and white cell counts were 213 × 10 /µL (IQR 142.0– diagnostic test (Access Bio Inc., New Jersey, USA, Cata- 3 3 3 287 × 10 /µL) and 5.8 × 10 /µL (IQR 4.5–7.0 × 10 /µL) logue number: G0141). The testing, results reading and respectively. interpretations were performed by strictly following the 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 χ 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 strains could be a possible reason for the difference seen Discussion in this study; more so because [19] realized a significant Malaria and typhoid are quite common in Tamale increase in the incidence of thrombocytopenia in P. fal- because the prevailing warm and humid climate is ciparum cases than in P. vivax cases. Our findings of a conducive for the infection, concomitant with poor higher prevalence and significant association of throm - sanitary practices that promote the infections [42]. bocytopenia with malaria adds to studies indicating that Malaria endemicity is nearly the same across the year 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 β Male 4 (28.6) 6 (60.0) 10 (71.4) 4 (40.0) 1.000 (0.244–3.574), 0.428 (0.439–11.530) Female 12 (30.0) 6 (40.0) 28 (70.0) 9 (60.0) α β 18–35 6 (16.7) 6 (54.5) 30 (83.3) 5 (45.5) 0.002 (0.009–0.346), 0.798 (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 β Male 6 (42.9) 0 (0.0) 8 (57.1) 10 (100.0) 0.723 (0.363–4.308), 0.051 (0.003–1.409) Female 15 (37.5) 6 (40.0) 25 (62.5) 9 (60.0) α β 18–35 14 (38.9) 3 (27.3) 22 (61.1) 8 (72.7) 0.349 (0.027–12.300), 0.114 (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 β Male 2 (14.3) 1 (10.0) 12 (85.7) 9 (90.0) 0.708 (0.108–3.053), 0.179 (0.017–1.680) Female 9 (22.5) 6 (40.0) 31 (77.5) 9 (60.0) α β 18–35 8 (22.2) 2 (18.2) 28 (77.8) 9 (81.8) 0.752 (0.248–21.110), 0.612 (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 β Male 3 (21.4) 1 (10.0) 11 (78.6) 9 (90.0) 0.358 (0.475–12.690), 1.000 (0.106–12.460) Female 4 (10.0) 1 (6.7) 36 (90.0) 14 (93.3) α β 18–35 2 (5.6) 1 (9.1) 34 (94.4) 10 (90.9) 0.057 (0.016–0.860), 0.811(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 β Male 0 (0.0) 0 (0.0) 14 (100.0) 10 (100.0) 0.560 (0.018–7.611), 1.000 (0.017–12.460) Female 3 (7.5) 1 (6.7) 37 (92.5) 14 (93.3) α β 18–35 2 (5.6) 1 (9.1) 34 (94.4) 10 (90.9) 0.589 (0.038–5.858), 0.811(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) 2 α β Source: Field Survey. *Analyzed using Pearson’s χ test or Fisher’s exact test, and represent 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 Additional files arrest and decrease in the number of erythroblasts as shown by [13]. The independence of the cytopenias Additional file 1. Document used in the collection of socio-demographic with typhoid, age and gender among the study popula- 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- taining data transribed from the questionnaire. Pancytopenia and bicytopenia are a common hema- tological problem encountered in clinical practice, which have multiple causes and the underlying pathol- Abbreviations ogy determines the management and prognosis of the 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- Authors’ contributions penias are seen in quite a number of malaria and 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. GKH supervised the study. All authors read and approved the final manuscript. agement of such cases, leading to earlier discharge of the patient. Unlike many studies that had male Author details dominance in pancytopenia cases [48–51], we real- Department of Biochemistry & Molecular Medicine, School of Medicine and Health Sciences, University for Development Studies, P. O. Box TL 1883, ized that pancytopenia was only found in females for Tamale, Ghana. 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 Acknowledgements with what pertains in Ghana, where women are more 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 Central Hospital for their immeasurable efforts. We also thank all our study in order to access treatment for themselves, which may 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 The authors declare that they have no competing interests. study, the worse form of cytopenia, pancytopenia is 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- script (Additional file 2). tions, the more damage the disease causes to one’s 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 ethical review board of the University for Development Studies, Ghana. Writ- topenia with malaria in adults in Tamale buttresses 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 Not applicable. Africa. The association of anemia with the middle aged adults with malaria should prompt a closer look at ane- Publisher’s Note mia with plasmodium infection in this age category in 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 Received: 3 November 2017 Accepted: 31 May 2018 28. Koram KA, et al. Seasonal profiles of malaria infection, anaemia, and bed- net use among age groups and communities in northern Ghana. Tropical Med Int Health. 2003;8(9):793–802. 29. Mockenhaupt FP, et al. Manifestation and outcome of severe malaria in children in northern Ghana. Am J Trop Med Hyg. 2004;71(2):167–72. 30. Squire DS, et al. Eec ff t of Plasmodium falciparum malaria parasites References on haematological parameters in Ghanaian children. J Parasit Dis. 1. Beck N. Pancytopenia and bicytopenia. In: Beck N, editor. Diagnostic 2016;40(2):303–11. hematology. New York: Springer; 2009. p. 297–308. 31. Mockenhaupt FP, et al. Anaemia in pregnant Ghanaian women: impor- 2. 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Published: Jun 5, 2018

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