• Users Online: 60
  • Print this page
  • Email this page


 
 
Table of Contents
ORIGINAL ARTICLE
Year : 2022  |  Volume : 5  |  Issue : 1  |  Page : 21-26

COVID-19 and anemia in children with nephrotic syndrome


1 Department of Pediatric Nephrology, Square Hospitals Ltd., Dhaka, Bangladesh
2 Department of Pediatric Nephrology, Dr. M. R. Khan Sishu Hospital and Institute of Child Health, Dhaka, Bangladesh
3 Department of Pediatric Nephrology, Chittagong Medical College Hospital, Chittagong, Bangladesh
4 Department of Pediatric Nephrology, Asgar Ali Hospital, Dhaka, Bangladesh
5 Department of Pediatric Nephrology, Dhaka Shishu (Children) Hospital, Dhaka, Bangladesh
6 Child Health Research Foundation, Dhaka, Bangladesh

Date of Submission18-Jul-2021
Date of Decision07-May-2022
Date of Acceptance12-May-2022
Date of Web Publication28-Jun-2022

Correspondence Address:
Md Abdul Qader
18/F, Bir Uttam Qazi Nuruzzaman Sarak, West Panthapath, Dhaka-1205
Bangladesh
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ajpn.ajpn_30_21

Rights and Permissions
  Abstract 


Context: Children with COVID-19 present with less severe disease and require fewer hospitalizations than adults. Our previous study on children with renal disease and COVID-19, which included predominantly children with nephrotic syndrome, found anemia in a significant number of participants. Aims: This study aimed at evaluating the risk factors of anemia in children with nephrotic syndrome presenting with COVID-19 and the influence of anemia on hospital outcome. Methods: This case–control study was conducted at five pediatric nephrology centers in two major cities of Bangladesh. Consecutive patients with nephrotic syndrome and positive polymerase chain reaction (PCR) for severe acute respiratory syndrome coronavirus 2 were included as cases, and subsequently, two cases of nephrotic syndrome with negative PCR were enrolled as controls. Participants who presented between April 2020 and December 2020 were included, and demographic data, clinical features, and laboratory parameters were retrieved from hospital records for analysis. Results: A total of 22 children with nephrotic syndrome were positive with COVID-19 and subsequently, 44 children were included as control. The median age was 6.4 years in the cases and 5.2 years among the control. Most children presented with the initial episode of nephrotic syndrome. The children in the case group had a significantly lower hemoglobin level than the controls, and anemia was associated with raised inflammatory markers. In multivariate analysis, female sex and impaired renal function was associated with lower hemoglobin, but anemia did not have effect on hospital outcome. Conclusions: Anemia in children can be multifactorial. Anemia in nephrotic syndrome associated with COVID-19 does not appear to influence length of hospital stay and outcome.

Keywords: Anemia, SARS-CoV2, acute kidney injury, inflammation, nephrotic syndrome


How to cite this article:
Qader MA, Sultana A, ul Quader MM, Rumana J, Khondaker T, Kanon N, Hanif M. COVID-19 and anemia in children with nephrotic syndrome. Asian J Pediatr Nephrol 2022;5:21-6

How to cite this URL:
Qader MA, Sultana A, ul Quader MM, Rumana J, Khondaker T, Kanon N, Hanif M. COVID-19 and anemia in children with nephrotic syndrome. Asian J Pediatr Nephrol [serial online] 2022 [cited 2022 Aug 18];5:21-6. Available from: https://www.ajpn-online.org/text.asp?2022/5/1/21/348527




  Introduction Top


Coronavirus disease (COVID-19), caused by severe acute respiratory syndrome coronavirus 2 (SARS CoV-2), was first detected in the Chinese province of Wuhan in 2019 and quickly spread worldwide.[1] It is an inflammatory condition defined by the release of pro-inflammatory cytokines linked to neutrophil activity, with the intensity of the inflammation worsening with age.[2] COVID-19 predominantly affects the respiratory system, but it has also been associated with a variety of cardiovascular and multisystem consequences, such as hepatic, cardiac, and kidney failure.[3],[4] Anemia is a prevalent symptom in COVID-19 patients. It is hypothesized to be caused by suppression of viral heme metabolism through surface glycoprotein binding to the beta chain of hemoglobin and virus-induced hemoglobin denaturation.[5],[6] Inflammation modifies iron homeostasis, such that there is increased iron acquisition and retention among macrophages and decreased bowel absorption.[7] This decreases the amount of iron available for erythropoiesis and hemoglobin synthesis. Furthermore, anemia of inflammation (AI) has previously been defined as a combination of cytokine-mediated erythropoiesis suppression, shortened erythrocyte half-life, and decreased erythropoietin biological activity.[8]

The presence of anemia has been proven to be a risk factor for a poor course and outcome in inflammation.[9],[10],[11],[12],[13] Anemia has been linked to severe COVID-19 and poor outcomes in adult populations, according to a study.[14] Our earlier study revealed significant anemia in children with preexisting renal disease who were admitted with a positive COVID-19 test.[15] The objective of this study was to evaluate anemia in children with nephrotic syndrome who were infected with COVID-19. Therefore, we designed a case–control study to evaluate the risk factors for anemia in children with nephrotic syndrome and COVID-19 infection and the influence of anemia on hospital outcome.


  Methods Top


This study is a follow-up to our prior work on the “Clinical profile and outcome of COVID-19 in children with preexisting renal disease.”[15] In the preceding study, we found that a significant number of children had anemia while hospitalized with COVID-19. Because the majority of the participants in the previous study had nephrotic syndrome, and anemia in nephrotic syndrome is uncommon, a case–control study was designed to identify the risk factors associated with developing anemia in the COVID-19-infected children, as well as the impact of anemia on hospital course and outcome.

Detection of COVID-19

All admitted patients were tested for COVID-19 for case identification and isolation regardless of their presenting symptoms to the hospital. A trained physician, nurse, or medical technologist collected a nasopharyngeal specimen, and the specimen was transferred to the laboratory immediately. Viral RNA was extracted from the nasopharyngeal specimen within 24–48 h of collection and tested for the presence of SARS-CoV2 using the COVID-19 reverse transcription–polymerase chain reaction (RT-PCR) kit (S3104E; Sansure Biotech Inc., Changsha, Hunan, China).

Selection of case and control

This case–control study was conducted on hospitalized children admitted to Dhaka Shishu Hospital, Dhaka, Dr M R Khan Shishu Hospital and Institute of Child Health, Dhaka, Chittagong Medical College Hospital, Chittagong, Square Hospitals Ltd., Dhaka, and Asgar Ali Hospital, Dhaka, between April 2020 and December 2020. This research work included children who had been diagnosed with nephrotic syndrome either before or after admission. The reasons for hospitalization of the patients with nephrotic syndrome were severe complications of relapse or relapse associated with severe infection. Children with a positive COVID-19 RT-PCR from a nasopharyngeal swab were included as cases. Patients with nephrotic syndrome who did not have COVID-19 infection were matched 1:2 from the admitted patients with matching of admission during the study period from the same institution, taking into consideration similar exposure potential, for the control group. As a result, when considering the issue of sample distribution, an age or gender match control could not be always considered. Controls were tested for COVID-19, and all were confirmed to be negative. Controls were recruited using a convenience sampling strategy, with two consecutive COVID-19 RT-PCR negative children from the hospital record being included as control after each positive case. Children with insufficient clinical details were excluded from the study.

Data collection

Clinical parameters included presenting characteristics, anthropometry and blood pressure at presentation, degree of anemia, signs of cardiac and respiratory dysfunction, organomegaly, and any rash. For the two groups, laboratory data such as complete blood count, iron profile, renal function test, liver function test, chest radiograph, and urine analysis were studied. Data on hospital stay and management, including the use of immunosuppressive drugs, antibiotics, and need for cardiorespiratory support, were included in the analysis.

Definition of anemia

The study employed the World Health Organization criteria of anemia, which defined anemia as hemoglobin <11 g/dL in children under the age of 5, <11.5 g/dL in children aged 5–11, and <12 g/dL in children aged 12 and over.[16] For purpose of the study, anemia was defined as hemoglobin levels <1 g/dL and categorized as no anemia, mild anemia, and moderate to severe anemia for hemoglobin values above 11 g/dL, between 9 and 11 g/dL, and below 9 g/dL, respectively.

Markers of inflammation and COVID-19

Because COVID-19 viral replication evokes inflammatory responses, resulting in monocyte and macrophage-induced cytokine and chemokines release,[17] we studied indicators such as C-reactive protein (CRP), procalcitonin, serum ferritin, erythrocyte sedimentation rate, and interleukin-6, which have been linked to severe COVID-19[18],[19],[20] to evaluate their association with the severity of anemia in patients with nephrotic syndrome and COVID-19.

Outcome measures

Various risk factors were examined for the association with anemia in patients with COVID-19 and nephrotic syndrome. Further, we evaluated whether length of hospital stay, requirements of respiratory support, and admission into intensive care unit were associated with anemia.

Statistical analysis

Data are presented using descriptive statistics, with continuous variables expressed as median (interquartile range, IQR) or mean ± standard deviation, based on the data distribution. Nonparametric Mann–Whitney U-test and Pearson Chi-square tests were used to compare demographic and laboratory characteristics between cases and controls. Multiple linear or logistic regression analysis was conducted to examine the association of risk factors with anemia among cases. Potential factors, chosen based on literature review, and examined for their association with severity and degree of anemia in COVID-19 patients, included sex; diagnosis; leukocyte, lymphocyte, and platelet counts; estimated glomerular filtration rate (eGFR); albumin; abnormalities on chest X-ray; and length of hospital stay. All tests were two-sided, and assessed at a level of significance of 0.1. SPSS Version 22.0 (SPSS Inc., Chicago, Illinois, USA) and Stata version 14.0 (Stata Corp LLC, Texas, USA).


  Results Top


Twenty-two children with nephrotic syndrome were positive for SARS-CoV2 infections during the study period at the five centers. Their demographic and clinical characteristics are depicted in [Table 1]. Half were boys, with slight male preponderance among controls. The median (IQR) age at presentation was 6.4 (4–9) years among the cases and 5.3 (3.7–7) years among the controls.
Table 1: Baseline characteristics and course of disease in inpatients with nephrotic syndrome

Click here to view


At admission 36% of the patients with COVID-19 (cases) and 53% of those without COVID-19 (controls) were in relapse of nephrotic syndrome, with or without infection. Both fever and cough were noted in 27% of the cases, while a few had only fever. The other important presenting feature was breathlessness (14%). At baseline, patients with COVID-19, when compared to controls, had lower median levels of hemoglobin (10.5 g/dL vs. 12.5 g/dL; P = 0.023) and eGFR (P = 0.049). Raised inflammatory markers were insignificantly more common among patients with COVID-19 (cases) than controls, including leukocytosis (leukocyte count >11,000/mm3; P = 0.85) and elevated CRP (>10 mg/L; P = 0.31).

About 42% of the cases had either pneumonia or pneumonia with pleural effusion in the chest radiograph. One-third of these required respiratory support, either in the form of nasal cannula or face mask [Table 1]. More than 80% of the cases and controls had good recovery within 15 days of hospital stay. Two (9%) of the 22 patients among the cases succumbed to sepsis and pulmonary edema; one patient also had septic shock.

Inflammatory indicators such as leukocytosis, neutrophilia, and raised CRP were associated with low hemoglobin levels (P = 0.025) among the cases versus controls. On bivariate analysis, lymphocytosis was linked to lower hemoglobin levels (P = 0.045) and higher eGFR (P = 0.027). Lymphocytosis was related to lower hemoglobin levels on bivariate analysis, and it remained significantly associated after adjusting for confounders such as gender, eGFR, and albumin.

As shown in [Table 2], on multiple regression, sex, a diagnosis of steroid-dependent or steroid-resistant nephrotic syndrome, lymphocytosis, thrombocytosis, and eGFR were significantly associated with degree of anemia among cases. The levels of hemoglobin were lower by approximately 2.25 g/dL among girls as compared to boys, after adjusting for other covariates (95% confidence interval [CI] −3.1,−1.4; P = 0.004). Patients with steroid-dependent or steroid-resistant nephrotic syndrome had higher hemoglobin levels, by 1.73 g/dL (P = 0.042) and 1.97 g/dL (P = 0.036), respectively, compared to the children with the initial episode of nephrotic syndrome. Children with thrombocytosis had lower hemoglobin, by 1.27 g/dL (95% CI − 2.371,−0.162; P = 0.036), in contrast to the children with normal platelet count, keeping all the covariates constant.
Table 2: Results of multiple regression analysis for the relationship between the degree of anemia and clinical parameters among the cases

Click here to view



  Discussion Top


As the pandemic progresses, with varying levels of penetration in different populations, our understanding of the disease's course and outcomes has improved tremendously. However, research on children with kidney disease was limited. Marlais et al. published a multinational study in which they looked at COVID-19 positive children who were receiving immunosuppressive therapy.[21] Their multicenter survey included 30 children with nephrotic syndrome, whereas our study included 22 children, indicating that children were less affected and required fewer COVID-19 admissions.[21] Adult patients with renal disease and a history of prior immunosuppressive therapy did not have an elevated risk of COVID-19 infection or severe disease due to immunosuppression, according to studies. Children and adolescents on immunosuppressants due to renal or other causes were also depicted in the studies with similar findings.[21],[22],[23],[24],[25] This is consistent with our findings and could explain why children on immunosuppression due to nephrotic syndrome had a decreased number of COVID-19 positive patients.

Considering above facts, this research has specifically examined the impact of COVID-19 on children with nephrotic syndrome. Earlier research in immunocompromised children revealed a milder infection with COVID-19.[21],[26] A systematic review found that SARS-CoV-2 infection among 43 children with idiopathic nephrotic syndrome was mild, less often required respiratory support and was not associated with death. However, the data in this analysis comes from developed countries.[27] Among the studied children, unfortunately we lost two patients. The first patient who was a case of infrequent relapse nephrotic syndrome who presented with sepsis, circulatory shock, and renal impairment and died within 24 h of admission. The second case presented with initial episode of the disease along with pneumonia and respiratory failure. In our study, the death rate was 11%. Other studies that included children on immunosuppressive medication found that mortality ranged from 0% to 28%.[28],[29],[30],[31],[32]

During the pandemic, parents were strict with their children in terms of severe home isolation and a delay in seeking medical help, which may have contributed to the deaths of those two children. During the COVID-19 pandemic, there have been instances of delayed hospitalization, as well as maltreatment or delayed treatment initiation.[33] On the other hand, a recent Latin American study on children with multisystem inflammatory syndrome found a strong link between mortality with immunodeficiency or use of immunosuppressive medicines.[34] Another study from the University Hospital Colorado's Department of Pediatrics found that being immunocompromised is a risk factor for admission, and that elevated CRP is linked to the requirement for critical care assistance.[35]

Our study had an important finding of lower degree of hemoglobin in COVID-19-positive cases in comparison to controls. The findings suggest that COVID-19 in children was not involving respiratory system alone, and may have multisystem involvement including sepsis which anemia of inflammation. Multivariate linear regression analysis among the COVID-19-positive cases revealed the presence of inflammation, abnormal or elevated renal function correlated with the degree of anemia. Surprisingly, girls were at risk of lower hemoglobin in multivariate linear regression analysis. Children who were either steroid-dependent nephrotic syndrome or steroid-resistant nephrotic syndrome, had higher hemoglobin in relation to those were at their initial episode or infrequent relapse. In a systematic review among adult patients, the authors found lower level of hemoglobin in older patients and those with diabetes mellitus and hypertension but not in those with kidney disease or on immunosuppression.[36] Another study revealed evidence of anemia in patients with heart failure.[37] Thrombocytosis was found to be significantly associated with anemia in multivariable regression analysis, which could be a result of viral infection, although the probability of iron deficiency could not be ruled out for all of the studied children.[38]

Important limitations of the study are the lack of investigations related to the cause of anemia and lack of evaluation of other anemia-related comorbidities. Detailed information regarding the past history of anemia and sociodemographic profile and dietary adequacy were lacking.


  Conclusions Top


Children with nephrotic syndrome who had COVID-19 had lower hemoglobin in comparison to their peers who were admitted without COVID-19. Raised inflammatory markers and impaired kidney function were risk factors for anemia. The degree of anemia did not influence the duration of hospital stay or mortality.

Acknowledgment

We thank all the members of the Departments of Pediatric Nephrology of all five institutes who helped us providing relevant data for this study.

Ethical clearance

Ethical clearance was taken from the institutional review board of Dhaka Sishu Hospital, Chittagong Medical College Hospital, Dr M. R. Khan Sishu Hospital and Institute of Child Health and hospital ethical committee of Square Hospitals Ltd and Asgar Ali Hospital before commencement of data collection from the institute.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Guan WJ, Ni ZY, Hu Y, Liang W, Ou C, Liu K, et al. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med 2020;382:1708-20.  Back to cited text no. 1
    
2.
Schouten LR, van Kaam AH, Kohse F, Veltkamp F, Bos LD, de Beer FM, et al. Age-dependent differences in pulmonary host responses in ARDS: A prospective observational cohort study. Ann Intensive Care 2019;9:55.  Back to cited text no. 2
    
3.
Bikdeli B, Madhavan MV, Jimenez D, Chuich T, Dreyfus I, Driggin E, et al. COVID-19 and thrombotic or thromboembolic disease: implications for prevention, antithrombotic therapy, and follow-up. J Am Coll Cardiol 2020;75:2950-73.  Back to cited text no. 3
    
4.
Zaim S, Chong JH, Sankaranarayanan V, Harky A. COVID-19 and multiorgan response. Curr Probl Cardiol 2020;45:100618.  Back to cited text no. 4
    
5.
Wenzhong L, Hualan L. COVID-19 disease: ORF8 and surface glycoprotein inhibit heme metabolism by binding to porphyrin. ChemRxiv 2020. [Preprint]. [doi: 10.26434/chemrxiv. 11938173.v3].  Back to cited text no. 5
    
6.
Wenzhong L, Hualan L. COVID-19 attacks the 1-beta chain of hemoglobin and captures the porphyrin to inhibit human heme metabolism. ChemRxiv 2020. [Preprint]. [doi: 10.26434/chemrxiv. 11938173.v8].  Back to cited text no. 6
    
7.
Theurl I, Aigner E, Theurl M, Nairz M, Seifert M, Schroll A, et al. Regulation of iron homeostasis in anemia of chronic disease and iron deficiency anemia: Diagnostic and therapeutic implications. Blood 2009;113:5277-86.  Back to cited text no. 7
    
8.
Weiss G, Ganz T, Goodnough LT. Anemia of inflammation. Blood 2019;133:40-50.  Back to cited text no. 8
    
9.
Cappellini MD, Comin-Colet J, de Francisco A, Dignass A, Doehner W, Lam CS, et al. Iron deficiency across chronic inflammatory conditions: International expert opinion on definition, diagnosis, and management. Am J Hematol 2017;92:1068-78.  Back to cited text no. 9
    
10.
Wouters HJ, van der Klauw MM, de Witte T, Stauder R, Swinkels DW, Wolffenbuttel BH, et al. Association of anemia with health-related quality of life and survival: A large population-based cohort study. Haematologica 2019;104:468-76.  Back to cited text no. 10
    
11.
Weiss G, Schett G. Anaemia in inflammatory rheumatic diseases. Nat Rev Rheumatol 2013;9:205-15.  Back to cited text no. 11
    
12.
Kurz K, Lanser L, Seifert M, Kocher F, Pölzl G, Weiss G. Anaemia, iron status, and gender predict the outcome in patients with chronic heart failure. ESC Heart Fail 2020;7:1880-90.  Back to cited text no. 12
    
13.
Wong MM, Tu C, Li Y, Perlman RL, Pecoits-Filho R, Lopes AA, et al. Anemia and iron deficiency among chronic kidney disease Stages 3-5ND patients in the Chronic Kidney Disease Outcomes and Practice Patterns Study: Often unmeasured, variably treated. Clin Kidney J 2020;13:613-24.  Back to cited text no. 13
    
14.
Bellman-Weiler R, Lanser L, Barket R, Rangger L, Schapfl A, Schaber M, et al. Prevalence and predictive value of anemia and dysregulated iron homeostasis in patients with COVID- 19 infection. J Clin Med 2020;9:2429.  Back to cited text no. 14
    
15.
Khondaker T, Qader MA, Gosh K, Chowdhury GN, Ferdous T, Afroz S, et al. Clinical profile and outcome of COVID -19 in children with pre-existing renal disease. J Ped Nephrol 2021;9:1-6.  Back to cited text no. 15
    
16.
WHO. Haemoglobin concentrations for the diagnosis of anemia and assessment of severity. Vitamin and Mineral Nutrition Information System. Geneva: World Health Organization; 2011 (WHO/NMH/NHD/MNM/11.1). Available from: http://www.who.int/vmnis/indicators/haemoglobin.pdf. [Last accessed on 2021 Apr 28].  Back to cited text no. 16
    
17.
Tay MZ, Poh CM, Rénia L, MacAry PA, Ng LF. The trinity of COVID-19: Immunity, inflammation and intervention. Nat Rev Immunol 2020;20:363-74.  Back to cited text no. 17
    
18.
Hu J, Wang Y. The Clinical Characteristics and Risk Factors of Severe Covid-19. Gerontology 2021;67:255–66. doi: 10.1159/000513400.  Back to cited text no. 18
    
19.
Gao Y, Li T, Han M, Li X, Wu D, Xu Y, et al. Diagnostic utility of clinical laboratory data determinations for patients with the severe COVID-19. J Med Virol 2020;92:791-6.  Back to cited text no. 19
    
20.
Qin C, Zhou L, Hu Z, Zhang S, Yang S, Tao Y, et al. Dysregulation of immune response in patients with coronavirus 2019 (COVID-19) in Wuhan, China. Clin Infect Dis 2020;71:762-8.  Back to cited text no. 20
    
21.
Marlais M, Wlodkowski T, Al-Akash S, Anamin P, Bandi VK, Baudouin V, et al. COVID-19 in children treated with immunosuppressive medication for kidney diseases. Arch Dis Child 2020;106:798-801.  Back to cited text no. 21
    
22.
Docherty AB, Harrison EM, Green CA, Hardwick HE, Pius R, Norman L, et al. Features of 20133 UK patients in hospital with COVID-19 using the ISARIC WHO clinical characterization protocol: Prospective observational cohort study. BMJ 2020;369:m1985.  Back to cited text no. 22
    
23.
Götzinger F, Santiago-García B, Noguera-Julián A, Lanaspa M, Lancella L, Calò Carducci FI, et al. COVID-19 in children and adolescents in Europe: A multinational, multicentre cohort study. Lancet Child Adolesc Health 2020;4:653-61.  Back to cited text no. 23
    
24.
Emmi G, Bettiol A, Mattioli I, Silvestri E, Di Scala G, Urban ML, et al. SARS-CoV-2 infection among patients with systemic autoimmune diseases. Autoimmun Rev 2020;19:102575.  Back to cited text no. 24
    
25.
Angeletti A, Drovandi S, Sanguineri F, Santaniello M, Ferrando G, Forno R, et al. COVID-19 in children with nephrotic syndrome on anti-CD20 chronic immunosuppression. Clin J Am Soc Nephrol 2020;15:1494-5.  Back to cited text no. 25
    
26.
Mantovani A, Rinaldi E, Zusi C, Beatrice G, Saccomani MD, Dalbeni A. Coronavirus disease 2019 (COVID-19) in children and/or adolescents: A meta-analysis. Pediatr Res 2021;89:733-7.  Back to cited text no. 26
    
27.
Morello W, Vianello FA, Proverbio E, Peruzzi L, Pasini A, Montini G. COVID-19 and idiopathic nephrotic syndrome in children: Systematic review of the literature and recommendations from a highly affected area. Pediatr Nephrol 2022;37:757-64.  Back to cited text no. 27
    
28.
Ketcham SW, Adie SK, Malliett A, Abdul-Aziz AA, Bitar A, Grafton G, et al. Coronavirus disease-2019 in heart transplant recipients in southeastern Michigan: A case series. J Card Fail 2020;26:457-61.  Back to cited text no. 28
    
29.
Fernandez-Ruiz M, Andrés A, Loinaz C, Delgado JF, López-Medrano F, San Juan R, et al. COVID-19 in solid organ transplant recipients: A single-center case series from Spain. Am J Transplant 2020;20:1849-58.  Back to cited text no. 29
    
30.
Pereira MR, Mohan S, Cohen DJ, Husain SA, Dube GK, Ratner LE, et al. COVID-19 in solid organ transplant recipients: Initial report from the US epicenter. Am J Transplant 2020;20:1800-8.  Back to cited text no. 30
    
31.
Columbia University Kidney Transplant Program. Early description of coronavirus 2019 disease in kidney transplant recipients in New York. J Am Soc Nephrol 2020;31:1150-6.  Back to cited text no. 31
    
32.
Banerjee D, Popoola J, Shah S, Ster IC, Quan V, Phanish M. COVID-19 infection in kidney transplant recipients. Kidney Int 2020;97:1076-82.  Back to cited text no. 32
    
33.
Lazzerini M, Barbi E, Apicella A, Marchetti F, Cardinale F, Trobia G. Delayed access or provision of care in Italy resulting from fear of COVID-19. Lancet Child Adolesc Health 2020;4:e10-1.  Back to cited text no. 33
    
34.
Antúnez-Montes OY, Escamilla MI, Figueroa-Uribe AF, Arteaga-Menchaca E, Lavariega-Saráchaga M, Salcedo-Lozada P, et al. COVID-19 and multisystem inflammatory syndrome in Latin American children: A multinational study. Pediatr Infect Dis J 2021;40:e1-6.  Back to cited text no. 34
    
35.
Graff K, Smith C, Silveira L, Jung S, Curran-Hays S, Jarjour J, et al. Risk factors for severe COVID-19 in children. Pediatr Infect Dis J 2021;40:e137-45.  Back to cited text no. 35
    
36.
Taneri PE, Gomez-Ochoa SA, Llanaj E, Raguindin PF, Rojas LZ, Roa-Díaz ZM, et al. Anemia and iron metabolism in COVID-19: A systemic review and meta-analysis. Eur J Epidemiol 2020;35:763-73.  Back to cited text no. 36
    
37.
Groenveld HF, Januzzi JL, Damman K, van Wijngaarden J, Hillege HL, van Veldhuisen DJ, et al. Anemia and mortality in heart failure patients a systematic review and meta-analysis. J Am Coll Cardiol 2008;52:818-27.  Back to cited text no. 37
    
38.
Tefferi A. In: Leung LL, Rosmarin AG, editors. Approach to the Patient with Thrombocytosis. UptoDate (Massachusetts, US) 2022; Available form: https://www. uptodate.com/contents/approach-to-the-patient-with-thrombocytosis?to picRef=6672&source=related_link#H1. [Last accessed on 2022 Feb 02; Last updated on 2022 Oct 02].  Back to cited text no. 38
    



 
 
    Tables

  [Table 1], [Table 2]



 

Top
 
  Search
 
    Similar in PUBMED
 Related articles
    Access Statistics
    Email Alert *
    Add to My List *
* Registration required (free)  

 
  In this article
Abstract
Introduction
Methods
Results
Discussion
Conclusions
References
Article Tables

 Article Access Statistics
    Viewed419    
    Printed8    
    Emailed0    
    PDF Downloaded52    
    Comments [Add]    

Recommend this journal