Case report
Managing hypertriglyceridemia in children with systemic lupus erythematosus: Two sides of the same coin
Manejo de la hipertrigliceridemia en niños con lupus eritematoso sistémico: 2 caras de la misma moneda
Biswanath Basu
, Binu George Babu, Suman Bhattacharyya
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Division of Pediatric Nephrology, Department of Pediatrics, NRS Medical College & Hospital, Kolkata, India
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Appropriate approval of our institutes’ ethical committee was obtained. Informed consent was obtained from parents of all individual participants included in the study.</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Case scenarios</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Case scenario 1</span><p id="par0010" class="elsevierStylePara elsevierViewall">An 11-year-old girl was admitted at our institute with anasarca, maculopapular rash over the face and hematuria (urine RBC plenty, urine protein–creatinine-ratio 1:7). Her blood pressure was normal for age, sex and height as per centile charts.<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">2</span></a> Investigations revealed mildly deranged renal function tests (BUN 88<span class="elsevierStyleHsp" style=""></span>mg/dl, creatinine 1.2<span class="elsevierStyleHsp" style=""></span>mg/dl) along with low C3 levels (35<span class="elsevierStyleHsp" style=""></span>mg/dl) and a positive ANA (titer >1:160), but complete blood count was unremarkable. She was also shown positive for anti-double-stranded DNA (dsDNA) (3+) and anti-nucleosome (3+) antibodies by immunofluorescence assay. Renal biopsy specimen confirmed changes of lupus nephritis stage II. Her lipid profile at presentation was serum triglyceride 172<span class="elsevierStyleHsp" style=""></span>mg/dl and serum cholesterol 233<span class="elsevierStyleHsp" style=""></span>mg/dl (HDL 44<span class="elsevierStyleHsp" style=""></span>mg/dl, LDL 106<span class="elsevierStyleHsp" style=""></span>mg/dl, VLDL 38<span class="elsevierStyleHsp" style=""></span>mg/dl). She was started on oral prednisolone (2<span class="elsevierStyleHsp" style=""></span>mg/kg/day), along with hydroxychloroquine (7<span class="elsevierStyleHsp" style=""></span>mg/kg/day) and rosuvastatin (5<span class="elsevierStyleHsp" style=""></span>mg/day) after obtaining due approval from her parents.</p><p id="par0015" class="elsevierStylePara elsevierViewall">We repeated investigations after one week of oral prednisolone and rosuvastatin usage. Surprisingly, lipid profile levels were found to be markedly elevated (triglyceride 1786<span class="elsevierStyleHsp" style=""></span>mg/dl, cholesterol 350<span class="elsevierStyleHsp" style=""></span>mg/dl, LDL 275<span class="elsevierStyleHsp" style=""></span>mg/dl, HDL 30<span class="elsevierStyleHsp" style=""></span>mg/dl and VLDL 88<span class="elsevierStyleHsp" style=""></span>mg/dl). She had also developed mild cushingoid features. Considering the possibility of an autoimmune phenomena, anti-lipoprotein-lipase (LPL) antibody (reactivity of anti-LPL immunoglobulin G was determined by enzyme-linked immunosorbent assay) estimation was done to find out the cause of hyperlipidemia. The report turned out to be negative. Hence, we were left with the possibility of steroid-induced hypertryglyceridemia. Prednisolone dose was rapidly tapered to 0.5<span class="elsevierStyleHsp" style=""></span>mg/kg/day. On serial follow-up, triglyceride levels of this child gradually reduced with decreasing doses of prednisolone (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>). At 4 weeks, her triglyceride level was 356<span class="elsevierStyleHsp" style=""></span>mg/dl and cholesterol was 222<span class="elsevierStyleHsp" style=""></span>mg/dl (HDL 38<span class="elsevierStyleHsp" style=""></span>mg/dl, LDL 146<span class="elsevierStyleHsp" style=""></span>mg/dl, VLDL 48<span class="elsevierStyleHsp" style=""></span>mg/dl). Mycophenolate mofetil (MMF) at a dose of 1000<span class="elsevierStyleHsp" style=""></span>mg/m<span class="elsevierStyleSup">2</span>/day was added to the schedule and prednisolone was continued at 0.5<span class="elsevierStyleHsp" style=""></span>mg/kg/day.</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Case scenario 2</span><p id="par0020" class="elsevierStylePara elsevierViewall">A 10-year-old girl was admitted to our pediatric emergency with hypertensive encephalopathy. She had also been suffering from low-grade intermittent fever, joint pains and a non-pruritic rash over exposed parts of the body, which worsened on exposure to sunlight. Strikingly, routine blood samples drawn in the emergency room were lipemic. Samples sent for determining lipid-profile revealed marked hypertriglyceridemia (serum triglyceride 4696<span class="elsevierStyleHsp" style=""></span>mg/dl) with hypercholesterolemia (serum cholesterol 514<span class="elsevierStyleHsp" style=""></span>mg/dl, HDL 24<span class="elsevierStyleHsp" style=""></span>mg/dl, LDL 357<span class="elsevierStyleHsp" style=""></span>mg/dl, VLDL 133<span class="elsevierStyleHsp" style=""></span>mg/dl). Complete blood counts revealed anemia (hemoglobin 8.7<span class="elsevierStyleHsp" style=""></span>mg/dl) with thrombocytopenia (1.2<span class="elsevierStyleHsp" style=""></span>lakh/cumm). Anti-nuclear (ANA, titer >1:160) and anti-ds DNA (3+) antibodies were positive. An MRI of the brain showed changes suggestive of acute disseminated encephalomyelilitis (ADEM). The child became fully conscious after successful control of hypertension over 48<span class="elsevierStyleHsp" style=""></span>h at our pediatric intensive care unit. In view of SLE with ADEM, pulse methyl-prednisolone (30<span class="elsevierStyleHsp" style=""></span>mg/kg/dose) was given for five days followed by oral prednisolone (2<span class="elsevierStyleHsp" style=""></span>mg/kg/day).</p><p id="par0025" class="elsevierStylePara elsevierViewall">Hydroxychloroquine (7<span class="elsevierStyleHsp" style=""></span>mg/kg/day), antihypertensives namely labetalol (1<span class="elsevierStyleHsp" style=""></span>mg/kg/dose) and amlodipine (10<span class="elsevierStyleHsp" style=""></span>mg/day), along with hypolipidemic agent rosuvastatin (5<span class="elsevierStyleHsp" style=""></span>mg/day) were also started along with fat-free diet. Due approval was obtained from the parents. Renal biopsy specimen confirmed changes of lupus nephritis stage II.</p><p id="par0030" class="elsevierStylePara elsevierViewall">In this case, repeat investigations after one week of prednisolone and rosuvastatin therapy revealed a mild improvement in lipid profile levels. Serum triglyceride reduced to 3851<span class="elsevierStyleHsp" style=""></span>mg/dl, cholesterol to 514<span class="elsevierStyleHsp" style=""></span>mg/dl, HDL to 24<span class="elsevierStyleHsp" style=""></span>mg/dl, LDL to 357<span class="elsevierStyleHsp" style=""></span>mg/dl and VLDL to 133<span class="elsevierStyleHsp" style=""></span>mg/dl. Another hypolipidemic agent, namely fenofibrate (45<span class="elsevierStyleHsp" style=""></span>mg/day) was added. Plasmapheresis was done to rapidly reduce the levels of circulating triglyceride levels to prevent inflammation of the pancreas. Anti-LPL antibody turned out to be positive (samples were considered positive if optical density was ≥3 standard deviations above the mean optical density obtained for the 20 control samples from healthy individuals included in each assay) this time. The dose of oral prednisolone was hiked to 3<span class="elsevierStyleHsp" style=""></span>mg/kg/day and MMF (800<span class="elsevierStyleHsp" style=""></span>mg/m<span class="elsevierStyleSup">2</span>/day) was also added. The child showed significant improvement in her lipid profile levels at the end of the second week (serum triglyceride 1435<span class="elsevierStyleHsp" style=""></span>mg/dl, cholesterol 234<span class="elsevierStyleHsp" style=""></span>mg/dl, HDL 54<span class="elsevierStyleHsp" style=""></span>mg/dl, LDL 237<span class="elsevierStyleHsp" style=""></span>mg/dl, VLDL 93<span class="elsevierStyleHsp" style=""></span>mg/dl) (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>). However, there was worsening of hypertension along some cushingoid-features due to the high-dose of prednisolone. So, we tapered the dose of prednisolone and increased the dose of MMF to 1200<span class="elsevierStyleHsp" style=""></span>mg/m<span class="elsevierStyleSup">2</span>/day. At 4-week follow-up, the child was normotensive on two antihypertensives and her lipid profiles significantly improved. Her serum triglyceride was 457<span class="elsevierStyleHsp" style=""></span>mg/dl and serum cholesterol was 184<span class="elsevierStyleHsp" style=""></span>mg/dl (HDL 74<span class="elsevierStyleHsp" style=""></span>mg/dl, LDL 137<span class="elsevierStyleHsp" style=""></span>mg/dl, VLDL 83<span class="elsevierStyleHsp" style=""></span>mg/dl) with decrease in the titer of anti-LPL antibody. Prednisolone was continued at a maintenance dose of 0.8<span class="elsevierStyleHsp" style=""></span>mg/kg/day.</p></span></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Discussion</span><p id="par0035" class="elsevierStylePara elsevierViewall">In this report, we have described two case scenarios with extreme hypertriglyceridemia in children with SLE. The first scenario was the more commonly encountered situation of steroid-induced hypertryglyceridemia, which was managed by tapering steroids and adding another immunosuppressant, MMF. The initial mild hyperlipidemia in this case may have been due to increased hepatic lipoprotein synthesis secondary to albuminuria.<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">3</span></a> Although it is common, the exact prevalence of steroid-induced hypertriglyceridemia is yet to be determined in the pediatric population. Studies show an increased tendency of lipid profiles in post-transplant patients treated with cyclosporine-prednisolone combination.<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">4</span></a> An experimental study on primates suggests that glucocorticoid-induced hypertriglyceridemia is primarily a consequence of increased hepatic-triglyceride production rates, through elevated plasma-free fatty acid and glucose levels.<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">5</span></a> However, exact mechanism of steroid-induced hypertriglyceridemia has not been definitely established.</p><p id="par0040" class="elsevierStylePara elsevierViewall">The second scenario depicts a situation where hypertriglyceridemia developed secondary to anti-LPL antibody. De Carvalho et al. found a prevalence of 46.7% of anti-LPL-antibodies in SLE in their study.<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">6</span></a> Anti-LPL antibodies have been closely linked to elevated triglyceride levels and implicated in mechanisms of atherosclerosis in SLE and other autoimmune inflammatory diseases such as rheumatoid arthritis and systemic sclerosis.<a class="elsevierStyleCrossRefs" href="#bib0085"><span class="elsevierStyleSup">7–9</span></a> This observation was explained on the basis of decreased LPL activity in these patients, which in turn corroborates with triglyceride levels.<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">7</span></a> Experimental studies have demonstrated that the association between autoimmune disease and LPL can lead to circulating LPL inhibitors, resulting in hyperchylomicronemia in patients with such diseases.<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">10</span></a> One study speculates that anti-LPL antibodies may be associated with disease activity and markers of inflammation in SLE.<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">6</span></a></p><p id="par0045" class="elsevierStylePara elsevierViewall">The present literature gives very little data on extreme hypertriglyceridemia in children with SLE. While most are iatrogenic and drug related, many can be due to developing autoantibodies against LPL. Our cases reveal two very different mechanisms as well as management for the same disease presentation. This report suggests that estimation of anti-LPL antibody is crucial in managing extreme hypertriglyceridemia with SLE. Detection of anti-LPL antibody level above the cut-off titer necessitates an increase in the dose of prednisolone or addition of another immunosuppressant. On the flip side, if the antibody titer is below cut-off value, then we may have to reduce the dose of prednisolone. Although extreme hypertriglyceridemia is generally well tolerated by most SLE patients, there is always the possibility of complications such as pancreatitis.<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">1</span></a> One other point of interest is the difficulty in controlling hypertriglyceridemia in these children with classical oral hypolipidemic agents.</p><p id="par0050" class="elsevierStylePara elsevierViewall">To conclude, hypertriglyceridemia in SLE can be due to two very different causes. An estimation of anti-LPL autoantibody level is useful in determining the next step of management.</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Ethical disclosures</span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Protection of human and animal subjects</span><p id="par0055" class="elsevierStylePara elsevierViewall">The authors declare that the procedures followed were in accordance with the regulations of the relevant clinical research ethics committee and with those of the Code of Ethics of the World Medical Association (Declaration of Helsinki).</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Confidentiality of data</span><p id="par0060" class="elsevierStylePara elsevierViewall">The authors declare that they have followed the protocols of their work center on the publication of patient data.</p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Right to privacy and informed consent</span><p id="par0065" class="elsevierStylePara elsevierViewall">The authors have obtained the written informed consent of the patients or subjects mentioned in the article. The corresponding author is in possession of this document.</p></span></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Financial support</span><p id="par0070" class="elsevierStylePara elsevierViewall">None.</p></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Authors’ contributions</span><p id="par0075" class="elsevierStylePara elsevierViewall">Dr. BG Babu, Dr. S Bhattacharyya & Dr. B Basu – case study, patient management, data collection and analysis, preparation of manuscript.</p></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Conflict of interest</span><p id="par0080" class="elsevierStylePara elsevierViewall">None.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:13 [ 0 => array:3 [ "identificador" => "xres976259" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec945932" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres976260" "titulo" => "Resumen" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0010" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec945933" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 5 => array:3 [ "identificador" => "sec0010" "titulo" => "Case scenarios" "secciones" => array:2 [ 0 => array:2 [ "identificador" => "sec0015" "titulo" => "Case scenario 1" ] 1 => array:2 [ "identificador" => "sec0020" "titulo" => "Case scenario 2" ] ] ] 6 => array:2 [ "identificador" => "sec0025" "titulo" => "Discussion" ] 7 => array:3 [ "identificador" => "sec0030" "titulo" => "Ethical disclosures" "secciones" => array:3 [ 0 => array:2 [ "identificador" => "sec0035" "titulo" => "Protection of human and animal subjects" ] 1 => array:2 [ "identificador" => "sec0040" "titulo" => "Confidentiality of data" ] 2 => array:2 [ "identificador" => "sec0045" "titulo" => "Right to privacy and informed consent" ] ] ] 8 => array:2 [ "identificador" => "sec0050" "titulo" => "Financial support" ] 9 => array:2 [ "identificador" => "sec0055" "titulo" => "Authors’ contributions" ] 10 => array:2 [ "identificador" => "sec0060" "titulo" => "Conflict of interest" ] 11 => array:2 [ "identificador" => "xack331165" "titulo" => "Acknowledgements" ] 12 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2016-07-13" "fechaAceptado" => "2016-09-08" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec945932" "palabras" => array:3 [ 0 => "Hypertriglyceridemia" 1 => "Systemic lupus erythematosus" 2 => "Lipoprotein lipase" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec945933" "palabras" => array:3 [ 0 => "Hipertrigliceridemia" 1 => "Lupus eritematoso sistémico" 2 => "Lipoproteína lipasa" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Hypertriglyceridemia is common in children with systemic lupus erythematosus (SLE). A retrospective analysis of the baseline clinical–pathological presentation and treatment outcome (status of lipid profiles) was performed in two children with SLE, who presented with extreme hypertriglyceridemia over a follow-up period of four weeks. The children were treated with prednisolone, mycophenolate mofetil (MMF), hydroxychloroquine and hypolipidemic agents, depending on their disease status. On serial follow-up, the first child showed a significantly raised serum triglyceride level after receiving one week of oral prednisolone therapy. Anti-lipoprotein-lipase (LPL) autoantibody was absent. Lipid profile levels of this child gradually improved after replacing oral prednisolone with another immunosuppressant, namely MMF. The second child presented with extreme hypertriglyceridemia with positive anti-LPL autoantibody. She responded to plasmapheresis followed by increasing the dose of immunosuppressant. So, extreme hypertriglyceridemia in children with SLE may be steroid induced or due to presence of anti-LPL auto antibody. Management should be individualized depending on the etiology.</p></span>" ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">La hipertrigliceridemia es común en niños con lupus eritematoso sistémico. Un análisis retrospectivo de la presentación clínico-patológica al inicio del estudio y los resultados del tratamiento (estado de los perfiles lipídicos) se llevó a cabo en 2 niños con lupus eritematoso sistémico, que presentaron hipertrigliceridemia extrema durante un período de seguimiento de 4 semanas. Los niños fueron tratados con prednisolona, micofenolatomofetil, hidroxicloroquina y agentes hipolipidemiantes, dependiendo de su estado de salud. En el seguimiento, el primer niño mostró un nivel de triglicéridos en suero significativamente elevado después de recibir una semana de tratamiento con prednisolona oral. No existían anticuerpos antilipoproteína lipasa. Los niveles de perfil de lípidos de este niño mejoraron gradualmente después de sustituir la prednisolona oral con otro inmunosupresor, a saber micofenolatomofetil. El segundo niño presentó hipertrigliceridemia extrema con autoanticuerpos antilipoproteína lipasa-positivos. Ella respondió a la plasmaféresis seguida del incremento de la dosis de inmunosupresores. Por lo tanto, la hipertrigliceridemia extrema en niños con lupus eritematoso sistémico puede ser inducida por esteroides o debido a la presencia de autoanticuerpos antilipoproteína lipasa. El manejo debe ser individualizado en función de la etiología.</p></span>" ] ] "multimedia" => array:1 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Fig. 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 956 "Ancho" => 1641 "Tamanyo" => 112324 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Serum triglyceride levels over time.</p>" ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:10 [ 0 => array:3 [ "identificador" => "bib0055" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Systemic lupus erythematosus associated with extreme hypertriglyceridemia" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:2 [ 0 => "C.S. 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Pitchumoni" ] ] ] ] ] "host" => array:1 [ 0 => array:1 [ "Revista" => array:6 [ "tituloSerie" => "J Clin Gastroenterol" "fecha" => "2003" "volumen" => "36" "paginaInicial" => "54" "paginaFinal" => "62" "link" => array:1 [ 0 => array:2 [ "url" => "https://www.ncbi.nlm.nih.gov/pubmed/12488710" "web" => "Medline" ] ] ] ] ] ] ] ] ] ] ] ] "agradecimientos" => array:1 [ 0 => array:4 [ "identificador" => "xack331165" "titulo" => "Acknowledgements" "texto" => "<p id="par0085" class="elsevierStylePara elsevierViewall">Dr. M Nandi and Prof. TKS Mahapatra.</p>" "vista" => "all" ] ] ] "idiomaDefecto" => "en" "url" => "/1699258X/0000001400000001/v2_201802071822/S1699258X16301085/v2_201802071822/en/main.assets" "Apartado" => array:4 [ "identificador" => "33643" "tipo" => "SECCION" "es" => array:2 [ "titulo" => "Casos clínicos" "idiomaDefecto" => true ] "idiomaDefecto" => "es" ] "PDF" => "https://static.elsevier.es/multimedia/1699258X/0000001400000001/v2_201802071822/S1699258X16301085/v2_201802071822/en/main.pdf?idApp=UINPBA00004M&text.app=https://reumatologiaclinica.org/" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S1699258X16301085?idApp=UINPBA00004M" ]
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