Skip to main content

Renal and hepatic dysfunction parameters correlate positively with gender among patients with recurrent malaria cases in Birnin Kebbi, Northwest Nigeria

Abstract

Background

Simultaneous increase in transaminases and bilirubin is an indicator of hepatic dysfunction in malaria. Malaria-induced hyperbilirubinemia has been associated with acute kidney injury and pathogenesis of cerebral malaria which are significantly associated with mortality in malaria infection. This retrospective study was designed to assess the lipid profile, and hematological, renal and hepatic function data of malaria patients in Sir Yahaya Memorial hospital Birnin Kebbi from 2016 to 2020 who are 18 years and above.

Methods

The data of all patients between 2016 and 2020 who are 18 years and above were collected. Complete data of 370 subjects who met the inclusion criteria which consist of 250 malaria subjects and 120 control subjects were analyzed.

Results

The results showed that females constitute 65.2% of malaria patients with complete records while the remaining 34.8% were males. Age distribution of the patients showed that the infection was more prevalent among 26–45 years and least among 65 years and above. Anemia and thrombocytopenia were prevalent among the female malaria patients compared to the male patients. Liver and kidney function parameters analyzed correlate positively with the gender. The infected male showed higher dysfunction in liver parameters while infected female patients showed significant dysfunction in kidney function parameters and lipid profile.

Conclusions

In conclusion, to prevent the potential widespread of acute renal and hepatic failure with the attendant morbidity and mortality among malaria patients, it is recommended that liver and kidney function tests be mandated for patients with recurring malaria and those with a history of treatment failure in the endemic area to ensure early diagnosis of malarial induced kidney and liver injury among malaria patients.

Highlights

• Liver and kidney dysfunction correlates positively with the gender.

• Infected male showed higher dysfunction in liver while female showed significant dysfunction in kidney

• Anaemia and thrombocytopenia were prevalent among the female malaria patients compare to the male

• There may be potential widespread of acute renal and hepatic if liver and kidney function tests are not mandated for patients with recurring malaria

Background

Malaria is an infectious disease of poverty of public health concern in subtropical and tropical regions [1]. Around 241 million cases of malaria with 627,000 deaths were reported in 2020 compared to 227 million cases in 2019. This represents an increase of around 14 million with an increase of 69,000 deaths above what was reported in 2019 [2]. About 90% of all the reported cases of malaria and deaths occur in Africa making Africa the epicenter of this disease [1, 3, 4]. It is of importance to note that one quarter of the malaria cases in Africa with the attendant mortality and morbidity occur in Nigeria [5]. If malaria infection is not treated on time, malaria parasites might obstruct blood flow to vital organs [6], invade and destroy vital organs [3], and induce biochemical and metabolic changes that may be detrimental to the host [7].

Malaria-induced hepatic injury is known to be a major feature of malaria and a major cause of morbidity and mortality in malaria patients [8,9,10]. Simultaneous increase in transaminases and bilirubin is considered as an indicator of liver dysfunction in malaria. Malaria-induced hyperbilirubinemia is associated with acute kidney injury and pathogenesis of acute renal failure among malaria patients [11,12,13,14,15]. This suggests that hepatic dysfunction is closely related to the development of acute kidney injury. In addition to this, malaria-induced hyperbilirubinemia has been implicated in the pathogenesis of cerebral malaria which is significantly associated with mortality in malaria infection, making it a serious concern in malaria patients [12, 16,17,18]. Malaria-induced hepatic damage impairs lipid homeostasis leading to alterations in host lipid and lipoprotein profiles which associate with the risk of cardiovascular disease in malaria patients [7, 19, 20]. This retrospective study of the clinical data of malaria patients with recurrent malaria cases attending Sir Yahaya Memorial Hospital Birnin Kebbi between 2016 and 2020 was conducted to determine the effect of malaria on the lipid profile, hematological, and renal and hepatic function parameters of the patients in order to prevent the occurrence of malaria-mediated liver and kidney injury in malaria patients.

Methods

Study area, study population, data collection, and preparation

The study was carried out in Birnin Kebbi Metropolis (12° 27′ 57.8808′′ N and 4° 11′ 58.2864′′ E.), Kebbi State in the Northern part of Nigeria. The data of all patients attending Sir Yahaya Memorial Hospital Birnin Kebbi, Kebbi State, between 2016 and 2020 who are 18 years and above were collected. The data of 370 subjects who met the inclusion criteria with complete lipid profile, renal, and hepatic data consisting of 250 malaria subjects and 120 control subjects were used for this study. Data were obtained directly from the medical record unit and the patient’s laboratory registration logbook using prepared data extraction sheet with the help of laboratory personnel. The data obtained include reporting date, age, sex, and laboratory results. Personal information of the patients such as name and address was not collected.

Exclusion criteria

Patients with pre-existing hepatic diseases, renal diseases, hypertension, human immunodeficiency virus, diabetes mellitus, acquired immune deficiency, viral hepatitis, drug-induced increase in liver and kidney biomarkers, and any condition that can affect the lipid profile, and all biomarkers being studied were not included in the study.

Ethical approval

Ethical approval was obtained from the hospital management before the commencement of data collection. The risk of loss of confidentiality was eliminated by the removal of personal identifiers and the use of identification numbers. All ethical procedures involving the use of human subjects under clinical settings were duly followed. The retrospective data was collected after ethical approval (SYMHBK/SUB/17/VOL.III/196) was obtained.

Statistical analysis

All statistical analyses were performed using GraphPad prism version 6 for Windows (GraphPad Software: San Diego, California, USA). The results were expressed as mean ± standard deviation. The differences in parameters across the groups were investigated using a one-way analysis of variance (ANOVA) followed by Tukey’s multiple comparison. P values <0.05 were considered significant while the difference within the group was analyzed using t test (p<0.05).

Results

Data of 250 malaria patients who are 18 years and above with a complete record for hematological parameters, lipid profile, and renal and hepatic dysfunction parameters from 2016 to 2020 in Sir Yahaya Memorial Hospital Birnin Kebbi, Kebbi State, who met the inclusion criteria were identified. One hundred sixty-three of these were females and 87 were males. That is, females composed 65.2% of malaria patients with complete records while the remaining 34.8% were males (Table 1). Most of the records of the patients contain the malaria test only in most cases. Although the other incomplete records were not used, females still constitute the higher percentage with malaria records in the health facility. For the control, more female records were also available to compare to males (Table 1). Age distribution of the infected patients showed that the infection was more prevalent among the age range 26–45 years which constitute 40.4% of the patients with a complete record followed by the 46–65 years of age bracket. People above 65 years constitute the least infected patients (Table 2).

Table 1 Gender profile of patients with recurrent malaria cases in sir Yahaya memorial hospital Birnin Kebbi from 2016 to 2020
Table 2 Age profile of patients with recurrent malaria cases in Sir Yahaya Memorial Hospital Birnin Kebbi from 2016 to 2020

Hemoglobin concentration, red blood cell counts, and packed cell volume were significantly (p<0.05) lower in malaria patients compared to the healthy patients. Moreover, the values were severely affected in the female patients compared to their male counterparts (Table 3). On the other hand, mean corpuscular hemoglobin concentration (MCHC) was significantly higher in patients than in non-malaria patients. It was also higher in female compared to male patients (Table 3). It showed that malaria-induced anemia was more profound in female malaria patients than in male patients. Significant (p<0.05) decrease in white blood cell count, platelets count, neutrophils, and monocytes was observed in all malaria patients compared to their respective control (Table 3). Significant (p<0.05) increase in lymphocytes was seen in both male and female malaria patients compared to their respective control (Table 3). Significant (p<0.05) reduction was more obvious among female malaria patients. Insignificant (p<0.05) increase was observed for the eosinophil and the basophil.

Table 3 Hematological profile of patients with recurrent malaria cases in sir Yahaya memorial hospital Birnin Kebbi from 2016 to 2020

Significant increase was observed in serum concentration of AST, ALT, ALP, total bilirubin, and direct bilirubin while a decrease in serum protein, albumin, and glucose was observed in the malaria patients (Table 4). In malaria infection studies, a simultaneous increase in transaminases and bilirubin is considered as an indicative of liver dysfunction. It seems the effect of the malaria infection on the liver function parameters analyzed correlates positively with the gender. Male tends to show higher dysfunction or compromise in these parameters than female.

Table 4 Liver function parameters and serum glucose profiles of patients with recurrent malaria cases in sir Yahaya memorial hospital Birnin Kebbi from 2016 to 2020

The renal function parameters of patients with recurrent malaria showed that there was a significant difference (p<0.05) between the serum creatinine concentrations of the malaria-infected patients compared to the control (Table 5). Moreover, the infected female patients also showed a significant elevated serum creatinine concentration compared to the infected males. The same results were observed for the serum urea of the patients compared with the control (Table 5). For the serum electrolytes, there was a significant reduction in sodium, potassium, and chloride level among the female patients compared to the control (Table 5). However, there was no significant (p<0.05) difference between the serum electrolytes of male malaria patients and the control (Table 5).

Table 5 renal function of patients with recurrent malaria cases in sir Yahaya memorial hospital Birnin Kebbi from 2016 to 2020

The analysis of the patient’s data revealed a statistical significant differences in the lipid profile of the patients compared with the control (Table 6). Significant (P<0.05) reduction in HDL, LDL, and TC was observed in malaria patients while a significant increase in triacylglycerol concentrations was found in malaria-infected patients compared to the control (Table 6).

Table 6 Lipid profile of patients with recurrent malaria cases in sir Yahaya memorial hospital Birnin Kebbi from 2016 to 2020

Discussion

From the hospital record, it was observed that prescription of other tests apart from malaria tests is usually recommended for people with recurrent malaria to ascertain the probable cause of treatment failure or other underlining conditions. The number of patients with complete records revealed that females are more likely to seek medical care in health facilities than men. The higher number of women with complete records than men was an indication that more women with recurrent malaria is coming back for follow-up than men. The higher rate of infection among females observed in this study agreed with Sakzabre et al. [21] who observed that females are more susceptible to malaria infection than males. However, Sacomboio et al. [22] and Adedapo et al. [23] observed that the higher prevalence among females may be linked to the fact that pregnant women are more affected by malaria and their inclusion in any study will always result in a higher prevalence among females than males. Since pregnant women are not excluded from the study, the higher rate of infection among women may be due to the inclusion of pregnant women in the study. This is contrary to the findings of Muddaiah and Prakash [24] who observed more cases among males (82%) compared to females (18%) in South Canara, South India, and Yadav et al. [25] who observed higher malaria infection among males (64.1%) than females (34.9%). In the Northern part of Nigeria, males who are the sole provider of the family in majority of the families are likely to be exposed to mosquito bites which increase their tendency of being infected with malaria. However, the tendency to get their medication over the counter than losing man hours in the hospital may be one of the reasons why less records of males were found in the health facility. This tendency has been observed in Saharan Africans by other researchers working with malaria patients [26,27,28,29]. In Nigeria, the acceptable adult age is 18 years and the retirement age is 60–65 years depending on the profession. This data shows that malaria mostly affects the active and young population in this region. This may partly explain the level of poverty in this region. It has also been observed from malaria studies in malaria-prone regions that people tend to acquire immunity against malaria over time. Therefore the susceptibility to infection may decrease as the patient grows. This may explain the low infection rate among adults above 60 years [30, 31].

Hematological abnormalities are well known to be the main features of malaria infection [32, 33], especially in P. falciparum infection that is common in Africa [34]. The changes observed in malaria infection are known to depend on many factors such as nutritional status, demographic factors, age, genetic susceptibility, hemoglobinopathy in patients, and malarial immunity [11, 35,36,37]. The study of the malaria patient data showed a significant decrease in hemoglobin concentration, red blood cell counts, and packed cell volume which indicate anemia. This is consistent with previous findings [38, 39]. In addition, an increase in mean corpuscular hemoglobin concentration (MCHC) was observed which is contrary to the other findings but in agreement with the findings of Kotepui et al. [40] who observed that significant reduction of hemoglobin, packed cell volume, and red blood cell counts which indicated anemia among the P. falciparum-infected malaria patients did not result in low MCHC as observed by other researchers. They discovered that P. falciparum infection resulted in the excessive release of immature red blood cells into blood circulation, which caused an increase in the value of MCHC while the patients were still anemic with a significant reduction of hemoglobin, packed cell volume, and red blood cell counts. In their earlier research, Kotepui et al. [41] also suggested that disease conditions like α+-thalassaemia among malaria patients can also result in the same observation. Anemia observed during malaria infection may be due to the destruction of infected erythrocytes, the removal of parasitized and non-parasitized erythrocytes. Studies on malaria therapy have revealed that for every infected red blood cells destroyed during the treatment of vivax and falciparum infection, 32 and 8 non-infected red blood cells respectively are also destroyed [42, 43]. This indiscriminate destruction of erythrocytes resulted from the effect of the antibodies generates against proteins on the red blood cell membrane during malaria infection which does not discriminate between non-parasitized and parasitized red blood cells. This eventually mediates the destruction of non-parasitized and parasitized red blood cells through immune-mediated lysis and phagocytosis [43,44,45,46,47]. The study also observed that the anemia was significantly higher among female malaria patients compared to the male patients making the females more vulnerable to anemia during malaria than the male patients. This was also observed by Sakzabre et al. [21] in their study.

In this study, thrombocytopenia was prevalent among the malaria patients with the female patients having a higher tendency to develop thrombocytopenia compare to the male patients. Similar results have been recorded in malaria research where a statistical significant correlation between malaria infection and thrombocytopenia has been established making thrombocytopenia a reliable predictor and reliable diagnostic marker of malaria infection and severity [31, 38, 41, 48,49,50,51,52]. The thrombocytopenia observed in malaria infection may be due to excessive removal of platelets by splenic pooling, peripheral destruction of platelets [47], malaria induce shortening of the life span of the platelets [31], antibody (IgG)-mediated platelet destruction [53], destruction by macrophages, platelet aggregation, and oxidative stress [54, 55]. A direct relationship between thrombocytopenia and the level of parasitemia and malaria positivity has also been reported [40, 56]. These make thrombocytopenia and anemia useful diagnostic standards for predicting the severity of malaria infection. This confirmed that females in this area are more prone to malaria than males [51, 57]. There was an increase in lymphocytes, eosinophils, and basophil in the patients but a significant decrease in white blood cells, neutrophils, and monocytes. Leucopenia is commonly associated with malaria infection [39, 48, 53, 58, 59]. Leucopenia is assumed to be due to the splenic sequestration and localization of leucocytes away from the peripheral circulation and other marginal pools rather than actual depletion or stasis [60], but leucocytosis has also been reported [61]. A significant decrease in neutrophils in malaria patients was observed in this study compared to the control. This is contrary to the findings of Maina et al. [39] and Kayode et al. [62].

The increase in lymphocytes observed among the patients in this study contradicts the reduction in lymphocytes observed by Kayode et al. [62] and Wickramasinghe and Abdalla [63].

A decrease in monocytes (monocytopenia) agreed with the findings of Bawah et al. [64] and Srivastava et al. [65] but contrary to the observation of Kotepui et al. [41]. Differences in observation may be due to the immune system of the host, level of parasitemia, severity of the infection, and co-infection.

The data obtained from the hospital records revealed a serious elevation in the liver enzymes and bilirubin in the patients irrespective of their gender compared to the control. This implied malaria-induced liver damage or dysfunction. This agrees with other studies that indicated a direct correlation between malaria and liver dysfunction. Liver dysfunction associated with malaria has been recognized as a major cause of malaria mortality and morbidity [3, 8, 10, 66,67,68,69]. Malaria-induced hyperbilirubinemia has been associated with acute kidney injury and pathogenesis of acute renal failure in malaria infection [11,12,13]. This suggests that hepatic dysfunction is closely related to the development of acute kidney disease. Severe hyperbilirubinemia in malaria infection has been implicated in the pathogenesis of cerebral malaria. Cerebral malaria is significantly associated with mortality in malaria infection, making hyperbilirubinemia a serious concern in malaria patients [12, 16, 17]. Malaria-induced hepatic damage has been linked to malaria-induced intravascular hemolysis induced by free heme overload [70]; systemic inflammation in response to malaria infection that aggravates the host hepatic tissue destruction [71] and the influx of IL-1α-producing neutrophil into the hepatocytes. The main source of IL-1α in the liver during malaria infection has been established to be the infiltrating neutrophils and not the other liver cell populations, though hepatocytes and Kupffer cells produce IL-1α during liver injury [72]. The neutrophils released IL-1α locally to promote the inflammatory response and TNF-α production that initiates apoptosis of hepatocytes [72]. Malaria infection has been shown to downregulate antioxidant gene expression in the liver [73,74,75]. This results in a reduced ability of the body to clear the free radicals and limit its ability to protect cellular constituents from oxidative damage. Drug-induced damage has been implicated also [76, 77]. Tissue damage leading to the level of serum biomarkers may also be related to reduced oxygen supply and disturbed metabolisms as a result of parasite sequestration in the microvascular capillary system [78]. This made Fazil et al. [67] to recommend liver function tests immediately after malaria is diagnosed in order to ensure early diagnosis of malarial-induced hepatic damage in patients.

This study showed a significant association between malaria infection and hypoglycemia. These findings agreed with the observation of Camara et al. [79] and Willcox et al. [80] who observed a direct link between mortality rate and hypoglycemia. Hypoglycemia in malaria infection is associated with hepatopathy [67]; malaria-induced cytokines [81]; and the use of drugs such as quinine [82], glucose consumption by the parasites during infections [83], and malnutrition [84, 85].

An increase in serum creatinine and urea was observed in the patients. Similar results have been obtained in other malaria studies [86,87,88]. Elevation of creatinine and urea concentration in the blood of the patients is an indication of possible renal dysfunction and degree of parasitemia in malaria patients [68, 86, 87]. Significant increase in renal disorder biomarkers in malaria patients is associated with vascular lesions triggered by medications, microorganisms, toxins, imbalance in the production of cytokines, endothelial adhesion, and increase glomerular cell proliferation [89,90,91,92]. Electrolyte abnormalities serve as an indicator of the severity of malaria in P. vivax and P. falciparum malaria which are the major species associated with major malaria cases in sub-Saharan African [5, 93]. This abnormality has been linked to malaria-induced acute kidney injury (AKI) [94, 95]. This study showed that malaria infection resulted in a reduction in a serum sodium level (hyponatremia) [5]. Reduction in serum sodium level has been observed in most cases of malaria and has been widely reported in P. falciparum and P. vivax infection, although it is commonly associated with P. falciparum malaria than P. vivax malaria [93, 96, 97]. These alterations in serum sodium concentration can result in several health conditions [5]. Malaria-induced vasopressin secretion is a major factor that results in the reduction in the concentration of sodium in malaria infection, as sodium is able to gain entry into the infected cells and cause loss of the blood [98]. Potassium imbalance can cause weakness and rapid heartbeat, therefore keeping the potassium level within the normal physiological level is very important [99]. The data of the patients clearly showed a decrease in serum potassium levels due to the malaria infection. This result is similar to the observation of [96]. This has been linked to malaria-induced enhanced urinary excretion of potassium leading to hypokalemia that is known to aggravate the complications associated with malaria infection [100]. A decrease in potassium is more common in P. falciparum infection compared to P. vivax infection [93].

Electrolyte abnormalities such as hyponatremia have been observed in 30–50% of cases of malaria-induced acute kidney injury (AKI) [94, 95] and are associated with hemolysis and acidosis [94]. Acute kidney injury (AKI) is gradually becoming a public health challenge in Africa due to the increase in the burden of diseases like malaria coupled with the late presentation of malaria patients for treatment and lack of medical resources for efficient care of patients who presented themselves to the health facilities. Acute kidney injury (AKI) has been reported in 1–4.8% of malaria patients in endemic areas and 25–30% in non-immune patients. This contributes to the high mortality rate of around 75% of malaria cases [92, 94, 101]. The autopsy on the kidney of patients who died of P. falciparum infection showed that half of the patients died of AKI [92].

Serum total cholesterol, HDL cholesterol, and LDL cholesterol were lower in the patients than in the controls. This is in contrast to some previous studies that reported elevation in cholesterol and these lipoproteins in the blood of malaria patients [102,103,104,105]. The reduction in HDL-cholesterol might be due to a decrease in cholesterol transport, inhibition of the liver enzyme by a parasite factor, uptake of the host cholesterol and phospholipids by the parasite, and esterification by lecithin cholesterol acyl transferase [106]. Oxidation of LDL cholesterol has been implicated in its reduction in malaria patients. This has been shown to increase the endothelial expression of adhesion molecules in malaria patients increasing the risk of cardiovascular disease in malaria patients [19]. Reduction in cholesterol levels in malaria patients is in support of earlier reports that hypocholesterolemia was significantly associated with malaria [107,108,109,110]. Increases in serum triacylglycerol (TG) were observed in the malaria patients compared to the healthy controls This might be due to increased mobilization of free fatty acids from adipose tissue [111], increases in hepatic fatty acid synthesis, impairment in lipoprotein lipase system, depression of fatty acid oxidation, and derived lipid from the phospholipids of the red blood cell membrane following hemolysis [112, 113].

Conclusion

Liver and kidney function parameters analyzed correlate positively with the gender. Infected males tend to show higher dysfunction in liver parameters while infected female patients showed a significant elevation in kidney dysfunction parameters. The positive correlation between gender and liver and kidney dysfunction needs to be analyzed further to see if other factors are involved. The result of this study showed that there is a danger of potential widespread acute renal and hepatic failure with the attendant morbidity and mortality. It is therefore recommended that liver and kidney function tests be recommended for patients with recurrent malaria and patients with failed self-medications in the endemic region to ensure early diagnosis of malarial-induced kidney and liver injury in malaria patients.

Availability of data and materials

The data used to support the findings of this study are available on request from the corresponding author.

Abbreviations

AST:

Aspartate aminotransferase

ALT:

Alanine aminotransferase

ALP:

Alkaline phosphatase

PCV:

Packed cell volume

MCHC:

Mean corpuscular hemoglobin concentration

RBC:

Red blood cell

WBC:

White blood cell

TC:

Total cholesterol

References

  1. Negatu GA, Abebe GA, Yalew WG (2022) Prevalence of malaria and associated factors among malaria-suspected patients attending Hamusit health center, Northwest Ethiopia: A cross-sectional study. J Parasitol Res 2022:1306049. https://doi.org/10.1155/2022/1306049

  2. Monroe A, Williams NA, Ogoma S, Karema C, Okumu F (2022) Reflections on the 2021 World Malaria Report and the future of malaria control. Malar J 21:154. https://doi.org/10.1186/s12936-022-04178-7

  3. Megabiaw F, Eshetu T, Kassahun Z, Aemero M (2022) Liver enzymes and lipid profile of malaria patients before and after antimalarial drug treatment at Dembia Primary Hospital and Teda Health Center, Northwest, Ethiopia. Res Rep Trop Med 13:11

    PubMed  PubMed Central  Google Scholar 

  4. Sacomboio ENM, Campos LH, Daniel FN, Ekundi-Valentin E (2021) Can vital signs indicate acute kidney injury in patients with malaria? Results of an observational study in Angola. Sci Afr 14:e01021

    CAS  Google Scholar 

  5. Ndako JA, Olisa JA, Ozoadibe OY, Dojumo VT, Fajobi VO et al (2020) Evaluation of the association between malaria infection and electrolyte variation in patients: use of Pearson correlation analytical technique. Inf Med Unlocked 21:100437

    Article  Google Scholar 

  6. Clark IA, Cowden WB (2003) The pathophysiology of falciparum malaria. Pharmacol Ther 99:221–260

    Article  CAS  PubMed  Google Scholar 

  7. Faucher J-F, Ngou-Milama E, Missinou M, Ngomo R, Kombila M et al (2002) The impact of malaria on common lipid parameters. Parasitol Res 88:1040–1043

    Article  PubMed  Google Scholar 

  8. Kochar D, Agarwal P, Kochar S, Jain R, Rawat N et al (2003) Hepatocyte dysfunction and hepatic encephalopathy in Plasmodium falciparum malaria. Qjm 96:505–512

    Article  CAS  PubMed  Google Scholar 

  9. Giannini EG, Testa R, Savarino V (2005) Liver enzyme alteration: a guide for clinicians. Cmaj 172:367–379

    Article  PubMed  PubMed Central  Google Scholar 

  10. Al-Salahy M, Shnawa B, Abed G, Mandour A, Al-Ezzi A (2016) Parasitaemia and Its relation to hematological parameters and liver function among patients malaria in Abs, Hajjah, Northwest Yemen. Interdisciplinary perspectives on infectious diseases 2016:5954394. https://doi.org/10.1155/2016/5954394

  11. Saravu K, Rishikesh K, Parikh CR (2014) Risk factors and outcomes stratified by severity of acute kidney injury in malaria. PLoS One 9:e90419

    Article  PubMed  PubMed Central  Google Scholar 

  12. Shukla VS, Singh RG, Rathore SS, Usha (2013) Outcome of malaria-associated acute kidney injury: a prospective study from a single center. Ren Fail 35:801–805

    Article  PubMed  Google Scholar 

  13. Bloom D, McCalden TA, Rosendorff C (1975) Effects of jaundiced plasma on vascular sensitivity to noradrenalin. Kidney Int 8:149–157

    Article  CAS  PubMed  Google Scholar 

  14. Cioffi W, DeMeules J, Kahng K, Wait R (1986) Renal vascular reactivity in jaundice. Surgery 100:356–362

    CAS  PubMed  Google Scholar 

  15. Baum M, Stirling G, Dawson J (1969) Further study into obstructive jaundice and ischaemic renal damage. Br Med J 2:229–231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Martins YC, Daniel-Ribeiro CT (2013) A new hypothesis on the manifestation of cerebral malaria: the secret is in the liver. Med Hypotheses 81:777–783

    Article  PubMed  Google Scholar 

  17. Dash S, Bhuyan U, Gupta A, Sharma L, Kumar A et al (1994) Falciparum malaria complicating cholestatic jaundice and acute renal failure. J Assoc Physicians India 42:101–102

    CAS  PubMed  Google Scholar 

  18. Prakash J, Gupta A, Kumar O, Rout SB, Malhotra V,  Srivastava PK (1996) Acute renal failure in falciparum malaria--increasing prevalence in some areas of India--a need for awareness.  Nephrol Dial Transplant 11(12):2414–2416. https://doi.org/10.1093/oxfordjournals.ndt.a027206

  19. Visser BJ, Wieten RW, Nagel IM, Grobusch MP (2013) Serum lipids and lipoproteins in malaria-a systematic review and meta-analysis. Malar J 12:1–16

    Article  Google Scholar 

  20. Sibmooh N, Yamanont P, Krudsood S, Leowattana W, Brittenham G et al (2004) Increased fluidity and oxidation of malarial lipoproteins: relation with severity and induction of endothelial expression of adhesion molecules. Lipids Health Dis 3:1–11

    Article  Google Scholar 

  21. Sakzabre D, Asiamah EA, Akorsu EE, Abaka-Yawson A, Dika ND et al (2020) Haematological profile of adults with malaria parasitaemia visiting the Volta Regional Hospital, Ghana. Adv Hematol 2020:9369758. https://doi.org/10.1155/2020/9369758

  22. Sacomboio ENM, dos Santos SC, Tchivango AT, Pecoits-Filho R, Calice-Silva V (2020) Does parasitemia level increase the risk of acute kidney injury in patients with malaria? Results from an observational study in Angola. Sci Afr 7:e00232

    Google Scholar 

  23. Adedapo AD, Falade CO, Kotila RT, Ademowo GO (2007) Age as a risk factor for thrombocytopenia and anaemia in children treated for acute uncomplicated falciparum malaria. J Vector Borne Dis 44:266

    PubMed  Google Scholar 

  24. Muddaiah M, Prakash P (2006) A study of clinical profile of malaria in a tertiary referral centre in South Canara. J Vector Borne Dis 43:29

    PubMed  Google Scholar 

  25. Yadav K, Dhiman S, Rabha B, Saikia P, Veer V (2014) Socio-economic determinants for malaria transmission risk in an endemic primary health centre in Assam, India. Infect Dis Poverty 3:1–8

    Article  Google Scholar 

  26. Chipwaza B, Mugasa JP, Mayumana I, Amuri M, Makungu C et al (2014) Self-medication with anti-malarials is a common practice in rural communities of Kilosa district in Tanzania despite the reported decline of malaria. Malar J 13:1–11

    Article  Google Scholar 

  27. Metta E, Haisma H, Kessy F, Hutter I, Bailey A (2014) “We have become doctors for ourselves”: motives for malaria self-care among adults in southeastern Tanzania. Malar J 13:1–13

    Article  Google Scholar 

  28. Kajeguka DC, Moses E (2017) Self-medication practices and predictors for self-medication with antibiotics and antimalarials among community in Mbeya City, Tanzania. Tanzan J Health Res 19(4). https://doi.org/10.4314/thrb.v19i4.6

  29. Lowassa A, Mazigo HD, Mahande AM, Mwang’onde BJ, Msangi S et al (2012) Social economic factors and malaria transmission in Lower Moshi, northern Tanzania. Parasit Vectors 5:1–9

    Article  Google Scholar 

  30. Bronzan RN, McMorrow ML, Patrick Kachur S (2008) Diagnosis of malaria. Mol Diagn Ther 12:299–306

    Article  PubMed  Google Scholar 

  31. Malik AM, Zaffar N, Ali N, Malik AM, Khan R (2010) Haematological findings and endemicity of malaria in Gadap region. J Coll Physicians Surg Pak 20:112–116

    PubMed  Google Scholar 

  32. Dalrymple U, Cameron E, Bhatt S, Weiss DJ, Gupta S et al (2017) Quantifying the contribution of Plasmodium falciparum malaria to febrile illness amongst African children. Elife 6:e29198

    Article  PubMed  PubMed Central  Google Scholar 

  33. Snow RW, Sartorius B, Kyalo D, Maina J, Amratia P et al (2017) The prevalence of Plasmodium falciparum in sub-Saharan Africa since 1900. Nature 550:515–518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Squire D, Asmah R, Brown C, Adjei D, Obeng-Nkrumah N et al (2016) Effect of Plasmodium falciparum malaria parasites on haematological parameters in Ghanaian children. J Parasit Dis 40:303–311

    Article  CAS  PubMed  Google Scholar 

  35. Price RN, Simpson JA, Nosten F, Luxemburger C, Hkirjaroen L et al (2001) Factors contributing to anemia after uncomplicated falciparum malaria. Am J Trop Med Hyg 65:614

    Article  CAS  PubMed  Google Scholar 

  36. Price RN, Douglas NM, Anstey NM (2009) New developments in Plasmodium vivax malaria: severe disease and the rise of chloroquine resistance. Curr Opin Infect Dis 22:430–435

    Article  PubMed  Google Scholar 

  37. Gupta P, Sharma R, Chandra J, Kumar V, Singh R et al (2016) Clinical manifestations and molecular mechanisms in the changing paradigm of vivax malaria in India. Infect Genet Evol 39:317–324

    Article  CAS  PubMed  Google Scholar 

  38. Osaro E, Jamilu MH, Ahmed H, Ezimah A (2014) Effect of plasmodium parasitaemia on some haematological parameters in children living in Sokoto, North Western, Nigeria. Int J Clin Med Res 1:57–64

    Google Scholar 

  39. Maina RN, Walsh D, Gaddy C, Hongo G, Waitumbi J et al (2010) Impact of Plasmodium falciparum infection on haematological parameters in children living in Western Kenya. Malar J 9:1–11

    Article  Google Scholar 

  40. Kotepui M, Piwkham D, PhunPhuech B, Phiwklam N, Chupeerach C et al (2015) Effects of malaria parasite density on blood cell parameters. PLoS One 10:e0121057

    Article  PubMed  PubMed Central  Google Scholar 

  41. Kotepui M, Phunphuech B, Phiwklam N, Chupeerach C, Duangmano S (2014) Effect of malarial infection on haematological parameters in population near Thailand-Myanmar border. Malar J 13:1–7

    Article  Google Scholar 

  42. Singh J, Purohit B, Desai A, Savardekar L, Shanbag P et al (2013) Clinical manifestations, treatment, and outcome of hospitalized patients with Plasmodium vivax malaria in two Indian states: a retrospective study. Malaria Res Treat 2013:341862. https://doi.org/10.1155/2013/341862

  43. Anstey NM, Russell B, Yeo TW, Price RN (2009) The pathophysiology of vivax malaria. Trends Parasitol 25:220–227

    Article  CAS  PubMed  Google Scholar 

  44. Hussain MM, Sohail M, Abhishek K, Raziuddin M (2013) Investigation on Plasmodium falciparum and Plasmodium vivax infection influencing host haematological factors in tribal dominant and malaria endemic population of Jharkhand. Saudi J Biol Sci 20:195–203

    Article  PubMed  PubMed Central  Google Scholar 

  45. Erhart LM, Yingyuen K, Chuanak N, Buathong N, Laoboonchai A et al (2004) Hematologic and clinical indices of malaria in a semi-immune population of western Thailand. Am J Trop Med Hyg 70:8–14

    Article  PubMed  Google Scholar 

  46. Gérardin P, Rogier C, Amadou SK, Jouvencel P, Brousse V et al (2002) Prognostic value of thrombocytopenia in African children with falciparum malaria. Am J Trop Med Hyg 66:686–691

    Article  PubMed  Google Scholar 

  47. Ladhani S, Lowe B, Cole AO, Kowuondo K, Newton CR (2002) Changes in white blood cells and platelets in children with falciparum malaria: relationship to disease outcome. Br J Haematol 119:839–847

    Article  PubMed  Google Scholar 

  48. George I, Ewelike-Ezeani C (2011) Haematological changes in children with malaria infection in Nigeria. J Med Med Sci 2:768–771

    Google Scholar 

  49. Jairajpuri ZS, Rana S, Hassan MJ, Nabi F, Jetley S (2014) An analysis of hematological parameters as a diagnostic test for malaria in patients with acute febrile illness: an institutional experience. Oman Med J 29:12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Ifeanyichukwu M, Esan A (2014) Evaluation of blood cells and platelets in Plasmodium falciparum malaria infected individuals. Int J Haematol Disord 1:49–54

    Google Scholar 

  51. Dhangadamajhi G, Panigrahi S, Roy S, Tripathy S (2019) Effect of Plasmodium falciparum infection on blood parameters and their association with clinical severity in adults of Odisha, India. Acta Trop 190:1–8

    Article  PubMed  Google Scholar 

  52. Aggarwal A, Rath S (2005) Plasmodium vivax malaria presenting with severe thrombocytopenia. J Trop Pediatr 51:120–121

    Article  PubMed  Google Scholar 

  53. Lathia T, Joshi R (2004) Can hematological parameters discriminate malaria from nonmalarious acute febrile illness in the tropics? Indian J Med Sci 58:239–244

    CAS  PubMed  Google Scholar 

  54. Autino B, Corbett Y, Castelli F, Taramelli D (2012) Pathogenesis of malaria in tissues and blood. Mediterr J Hematol Infect Dis 4(1):e2012061. https://doi.org/10.4084/MJHID.2012.061

  55. Lacerda MVG, Mourão MPG, Coelho HCC, Santos JB (2011) Thrombocytopenia in malaria: who cares? Mem Inst Oswaldo Cruz 106:52–63

    Article  PubMed  Google Scholar 

  56. Igbeneghu C, Odaibo A (2013) Impact of acute malaria on some haematological parameters in a semi-urban community in southwestern Nigeria. Acta Parasitol Globalis 4:01–05

    Google Scholar 

  57. Nlinwe NO, Nange TB (2020) Assessment of hematological parameters in malaria, among adult patients attending the Bamenda Regional Hospital. Anemia 2020:3814513. https://doi.org/10.1155/2020/3814513

  58. Ovuakporaye S (2011) Effect of malaria parasite on some haematological parameters: red blood cell count, packed cell volume and haemoglobin concentration. J Med Appl Biosci 3:45–51

    Google Scholar 

  59. Warimwe GM, Murungi LM, Kamuyu G, Nyangweso GM, Wambua J et al (2013) The ratio of monocytes to lymphocytes in peripheral blood correlates with increased susceptibility to clinical malaria in Kenyan children. PLoS One 8:e57320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. McKenzie FE, Prudhomme WA, Magill AJ, Forney JR, Permpanich B et al (2005) White blood cell counts and malaria. J Infect Dis 192:323–330

    Article  PubMed  Google Scholar 

  61. Modiano D, Sirima BS, Konaté A, Sanou I, Sawadogo A (2001) Leucocytosis in severe malaria. Trans R Soc Trop Med Hyg 95:175–176

    Article  CAS  PubMed  Google Scholar 

  62. Kayode O, Kayode A, Awonuga O (2011) Status of selected hematological and biochemical parameters in malaria and malaria-typhoid co-infection. J Biol Sci 11:367–373

    Article  CAS  Google Scholar 

  63. Wickramasinghe SN, Abdalla SH (2000) Blood and bone marrow changes in malaria. Best Pract Res Clin Haematol 13:277–299

    Article  CAS  Google Scholar 

  64. Bawah AT, Nyakpo KT, Ussher FA, Alidu H, Dzogbo JJ et al (2018) Hematological profile of children under five years with malaria at the ho municipality of Ghana. Edorium. J Pediatr 2:100004P05AB2018

  65. Srivastava S, Jain P, Kuber D, Sharma G (2011) Haematological profile of vivax malaria patients. Age 29:11–15

    Google Scholar 

  66. Kausar MW, Moeed K, Asif N, Rizwi F, Raza S (2010) Correlation of bilirubin with liver enzymes in patients of falciparum malaria. Int J Pathol 8:63–67

    Google Scholar 

  67. Fazil A, Vernekar PV, Geriani D, Pant S, Senthilkumaran S et al (2013) Clinical profile and complication of malaria hepatopathy. J Infect Public Health 6:383–388

    Article  PubMed  Google Scholar 

  68. Tovar-Acero C, Velasco MC, Avilés-Vergara PA, Ricardo-Caldera DM, Alvis EM et al (2021) Liver and kidney dysfunction, hypoglycemia, and thrombocytopenia in Plasmodium vivax malaria patients at a Colombian Northwest region. Parasite Epidemiol Control 13:e00203

    Article  PubMed  PubMed Central  Google Scholar 

  69. Kaeley N, Ahmad S, Shirazi N, Bhatia R, Bhat NK et al (2017) Malarial hepatopathy: a 6-year retrospective observational study from Uttarakhand, North India. Trans R Soc Trop Med Hyg 111:220–225

    Article  CAS  PubMed  Google Scholar 

  70. Dey S, Bindu S, Goyal M, Pal C, Alam A et al (2012) Impact of intravascular hemolysis in malaria on liver dysfunction: involvement of hepatic free heme overload, NF-κB activation, and neutrophil infiltration. J Biol Chem 287:26630–26646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Liaskou E, Wilson DV, Oo YH (2012) Innate immune cells in liver inflammation. Mediators Inflamm 2012:949157.  https://doi.org/10.1155/2012/949157

  72. de Menezes MN, Salles ÉM, Vieira F, Amaral EP, Zuzarte-Luís V et al (2019) IL-1α promotes liver inflammation and necrosis during blood-stage Plasmodium chabaudi malaria. Sci Rep 9:1–12

    Article  Google Scholar 

  73. Reuling IJ, Van De Schans LA, Coffeng LE, Lanke K, Meerstein-Kessel L et al (2018) A randomized feasibility trial comparing four antimalarial drug regimens to induce Plasmodium falciparum gametocytemia in the controlled human malaria infection model. Elife 7:e31549

    Article  PubMed  PubMed Central  Google Scholar 

  74. Srivastava P, Arif AJ, Pandey VC (1995) Status of hepatic glutathione-S-transferase (s) during Plasmodium berghei infection and chloroquine treatment in Mastomys natalensis. Int J Parasitol 25(2):203–205. https://doi.org/10.1016/0020-7519(94)00089-7

  75. Siddiqi NJ, Pandey VC (1999) Studies on hepatic oxidative stress and antioxidant defence systems during artemether treatment of Plasmodium yoelii nigeriensis infected mice. Mol cell biochem 196(1-2):169–173.

  76. Duparc S, Borghini-Fuhrer I, Craft CJ, Arbe-Barnes S, Miller RM et al (2013) Safety and efficacy of pyronaridine-artesunate in uncomplicated acute malaria: an integrated analysis of individual patient data from six randomized clinical trials. Malar J 12:1–18

    Article  Google Scholar 

  77. Silva-Pinto A, Ruas R, Almeida F, Duro R, Silva A et al (2017) Artemether-lumefantrine and liver enzyme abnormalities in non-severe Plasmodium falciparum malaria in returned travellers: a retrospective comparative study with quinine-doxycycline in a Portuguese centre. Malar J 16:1–5

    Article  Google Scholar 

  78. Anand AC, Puri P (2005) Jaundice in malaria. J Gastroenterol Hepatol 20:1322–1332

    Article  PubMed  Google Scholar 

  79. Camara B, Diagne-Gueye N, Faye P, Fall M, Ndiaye J et al (2011) Malaria severity criteria and prognostic factors among children in Dakar. Med Mal Infect 41:63–67

    Article  CAS  PubMed  Google Scholar 

  80. Willcox ML, Forster M, Dicko MI, Graz B, Mayon-White R et al (2010) Blood glucose and prognosis in children with presumed severe malaria: is there a threshold for ‘hypoglycaemia’? Trop Med Int Health 15:232–240

    Article  CAS  PubMed  Google Scholar 

  81. Rockett K, Awburn M, Rockett E, Clark I (1994) Tumor necrosis factor and interleukin-1 synergy in the context of malaria pathology. Am J Trop Med Hyg 50:735–742

    Article  CAS  PubMed  Google Scholar 

  82. Bartoloni A, Zammarchi L (2012) Clinical aspects of uncomplicated and severe malaria. Mediterr J Hematol Infect Dis 4(1):e2012026. https://doi.org/10.4084/MJHID.2012.026

  83. Madrid L, Lanaspa M, Maculuve SA, Bassat Q (2015) Malaria-associated hypoglycaemia in children. Expert Rev Anti Infect Ther 13:267–277

    Article  CAS  PubMed  Google Scholar 

  84. Sambany E, Pussard E, Rajaonarivo C, Raobijaona H, Barennes H (2013) Childhood dysglycemia: prevalence and outcome in a referral hospital. PLoS One 8:e65193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Lanneaux J, Dauger S, Pham L-L, Naudin J, Faye A et al (2016) Retrospective study of imported falciparum malaria in French paediatric intensive care units. Arch Dis Child 101:1004–1009

    Article  PubMed  Google Scholar 

  86. Afrifa J, Essien-Baidoo S, Baffour Gyau A, Ephraim RKD (2017) Evaluation of renal function in pregnant women with malaria: a case-control study in a mesoendemic area. Obstet Gynecol Int 2017:6030943. https://doi.org/10.1155/2017/6030943

  87. Ekeanyanwu RC, Ogu GI (2010) Assessment of renal function of Nigerian children infected with Plasmodium falciparum. Int J Med Med Sci 2:251–255

    CAS  Google Scholar 

  88. Ogbadoyi EO, Tsado RD (2009) Renal and hepatic dysfunction in malaria patients in Minna, North Central Nigeria. Online J Health Allied Sci 8(3):8. http://www.ojhas.org/issue31/2009-3-8.htm

  89. Sinha A, Singh G, Bhat AS, Mohapatra S, Gulati A et al (2013) Thrombotic microangiopathy and acute kidney injury following vivax malaria. Clin Exp Nephrol 17:66–72

    Article  PubMed  Google Scholar 

  90. Yeo TW, Lampah DA, Tjitra E, Piera K, Gitawati R et al (2010) Greater endothelial activation, Weibel-Palade body release and host inflammatory response to Plasmodium vivax, compared with Plasmodium falciparum: a prospective study in Papua, Indonesia. J Infect Dis 202:109–112

    Article  CAS  PubMed  Google Scholar 

  91. Toshan NC, Tundwal VK, Aswal VK, Gahlot NK, Meena MK et al (2016) Spectrum of renal dysfunction in malaria. Int J Mosquito Res 3:9–13

    Google Scholar 

  92. Wichapoon B, Punsawad C, Chaisri U, Viriyavejakul P (2014) Glomerular changes and alterations of zonula occludens-1 in the kidneys of Plasmodium falciparum malaria patients. Malar J 13:1–10

    Article  Google Scholar 

  93. Jasani JH, Sancheti SM, Gheewala BS, Bhuva KV, Doctor VS et al (2012) Association of the electrolyte disturbances (Na+, K+) with the type and severity of the malarial parasitic infection. J Clin Diagn Res 6:678–681

    CAS  Google Scholar 

  94. Barsoum RS (2000) Malarial acute renal failure. J Am Soc Nephrol 11:2147–2154

    Article  PubMed  Google Scholar 

  95. Naqvi R, Akhtar F, Ahmed E, Sheikh R, Bhatti S et al (2016) Malarial acute kidney injury: 25 years experience from a center in an endemic region. Br J Med Med Res 12:1

    Article  Google Scholar 

  96. Ikekpeazu EJ, Neboh EE, Aguchime NC, Maduka IC, Anyanwu EG (2010) Malaria parasitaemia: effect on serum sodium and potassium levels. Biol Med 2:20–25

    CAS  Google Scholar 

  97. Olaniyan M (2005) The pattern of packed cell volume, plasma electrolytes and glucose levels in patients infected with Plasmodium falciparum. Afr J Clin Exp Microbiol 6:87–90

    Google Scholar 

  98. Hanson J, Hossain A, Charunwatthana P, Hassan MU, Davis TM et al (2009) Hyponatremia in severe malaria: evidence for an appropriate anti-diuretic hormone response to hypovolemia. Am J Trop Med Hyg 80:141

    Article  PubMed  PubMed Central  Google Scholar 

  99. Peterson LN (1997) Potassium in nutrition. In: Handbook of nutritionally essential minerals, pp 153–183

    Google Scholar 

  100. Baloch S, Memon S, Gachal G, Baloch M (2011) Determination of trace metals abnormalities in patients with vivax malaria. Iran J Parasitol 6:54

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Silva GB, Pinto JR, Barros EJG, Farias GMN, Daher EDF (2017) Kidney involvement in malaria: an update. Rev Inst Med Trop Sao Paulo 59:e53. https://doi.org/10.1590/S1678-9946201759053

  102. Nilsson-Ehle I, Nilsson-Ehle P (1990) Changes in plasma lipoproteins in acute malaria. J Intern Med 227:151–155

    Article  CAS  PubMed  Google Scholar 

  103. Davis T, Sturm M, Zhang Y-R, Spencer J, Graham R et al (1993) Platelet-activating factor and lipid metabolism in acute malaria. J Infect 26:279–285

    Article  CAS  PubMed  Google Scholar 

  104. Vial HJ, Eldin P, Tielens AG, van Hellemond JJ (2003) Phospholipids in parasitic protozoa. Mol Biochem Parasitol 126:143–154

    Article  CAS  PubMed  Google Scholar 

  105. Ndukaku OY, Ejiofor E, Loveth UE, Oluchi OI (2015) Valuation of some serum kidney functions and lipid profile of malaria patients in South Eastern Nigeria. Rom J Biochem 52:39–49

    Google Scholar 

  106. Krishna AP, Chandrika KS, Acharya M, Patil SL (2009) Variation in common lipid parameters in malaria infected patients. Indian J Physiol Pharmacol 53:271–274

    CAS  PubMed  Google Scholar 

  107. Grellier P, Rigomier D, Clavey V, Fruchart J-C, Schrevel J (1991) Lipid traffic between high density lipoproteins and Plasmodium falciparum-infected red blood cells. J Cell Biol 112:267–277

    Article  CAS  PubMed  Google Scholar 

  108. Miller LH, Baruch DI, Marsh K, Doumbo OK (2002) The pathogenic basis of malaria. Nature 415:673–679

    Article  CAS  PubMed  Google Scholar 

  109. Badiaga S, Barrau K, Parola P, Brouqui P, Delmont J (2002) Contribution of nonspecific laboratory test to the diagnosis of malaria in febrile travelers returning from endemic areas: value of hypocholesterolemia. J Travel Med 9:117–121

    Article  PubMed  Google Scholar 

  110. Sirak S, Fola AA, Worku L, Biadgo B (2016) Malaria parasitemia and its association with lipid and hematological parameters among malaria-infected patients attending at Metema Hospital, Northwest Ethiopia. Pathol Lab Med Int 8:43–50

    Article  Google Scholar 

  111. Akanbi O, Badaki J, Adeniran O, Olotu O (2010) Effect of blood group and demographic characteristics on malaria infection, oxidative stress and haemoglobin levels in South Western Nigeria. Afr J Microbiol Res 4:877–880

    CAS  Google Scholar 

  112. Bansal D, Bhatti HS, Sehgal R (2005) Role of cholesterol in parasitic infections. Lipids Health Dis 4:1–7

    Article  Google Scholar 

  113. Bouyou-Akotet M, Mawili Mboumba D, Guiyedi V, Pemba Mihindou M, Maryvonne Kombila M (2014) Altered total cholesterol and triglyceride levels during the course of Plasmodium falciparum infection in children. J Parasitol Vector Biol 6:174–180

    Article  Google Scholar 

Download references

Acknowledgements

The authors express their gratitude to the management of Sir Yahaya Memorial Hospital Birnin Kebbi, Kebbi State, Nigeria. We are also grateful to all the laboratory staff and staff at the Medical Record Department of Sir Yahaya Memorial Hospital Birnin Kebbi, Kebbi State, for their effort during the data collection.

Consent to participate

Not applicable, since the study is retrospective.

Funding

Not applicable.

Author information

Authors and Affiliations

Authors

Contributions

ORJ designed the study; ORJ and JIG collected the data; ORJ, JIG, ADM, GG, and LIY analyzed and interpreted the data; ORJ and JIG wrote the first draft manuscript; ORJ, GG, ADM, and LIY performed the critical revisions of the manuscript; LIY, ADM, and GG provided the administrative, technical, and material support; ORJ coordinated and supervised the study. The the authors read and approved the final manuscript.

Corresponding author

Correspondence to Rotimi Johnson Ojo.

Ethics declarations

Ethics approval and consent to participate

Ethical approval was obtained from the hospital management before the commencement of data collection. The risk of loss of confidentiality was eliminated by the removal of personal identifiers and the use of identification numbers. All ethical procedures involving the use of human subjects under clinical settings were duly followed. The retrospective data was collected after ethical approval (SYMHBK/SUB/17/VOL.III/196) was obtained.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ojo, R.J., Jonathan, I.G., Adams, M.D. et al. Renal and hepatic dysfunction parameters correlate positively with gender among patients with recurrent malaria cases in Birnin Kebbi, Northwest Nigeria. Egypt J Intern Med 34, 77 (2022). https://doi.org/10.1186/s43162-022-00164-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s43162-022-00164-2

Keywords