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1 Clinical Pediatric Hematology-Oncology Volume ㆍ Number ㆍ October 04 ORIGINAL ARTICLE 소아청소년기에발생한중증호중구감소증의관찰 이진희 ㆍ김소현 ㆍ김성구 ㆍ이재욱 ㆍ장필상 ㆍ김명신 ㆍ정낙균 ㆍ조빈 ㆍ김학기 가톨릭대학교의과대학 소아과학교실, 가톨릭유전진단검사센터진단검사의학교실 Clinical and Laboratory Features of Severe Neutropenia Developed in Childhood Jin Hee Lee, M.D., So Hyun Kim, M.D., Sung Koo Kim, M.D., Jae Wook Lee, M.D., Pil-Sang Jang, M.D., Myungshin Kim, M.D., Nack-Gyun Chung, M.D., Bin Cho, M.D. and Hack-Ki Kim, M.D. Department of Pediatrics, Laboratory Medicine and Catholic Genetic Laboratory Center, The Catholic University of Korea, College of Medicine, Seoul, Korea Background: Neutropenia is not uncommon in children. We performed this study to investigate the etiology, clinical course and laboratory characteristics for prediction of recovery in children with severe neutropenia. Methods: In this study, we studied the clinical course and hematological features of 07 patients with severe neutropenia who were diagnosed and treated at the Department of Pediatrics, The Catholic University of Korea from April 009 to July 04. Patients with hematologic disorders and malignant disease were excluded. Chronic severe neutropenia (CSN) was defined as an absolute neutrophil count of /L or less for at least months. Acute severe neutropenia (ASN) were defined who recovered within months from diagnosis. Results: Among 07 patients, 7 patients showed ASN and 5 patients were CSN. Median age of ASN (5. months) was higher than that of CSN (0.7 months). The median duration of recovery from neutropenia was 7 days (range: -5) in ASN. ASN was commonly related to infectious diseases and 4 cases (.%) had documented etiologic agents. Median duration of recovery from neutropenia was 8 months in CSN. Three of 5 patients in CSN had ELANE gene mutation. The number of white blood cells, platelets, monocytes, and eosinophils were significantly higher in group of CSN compared with ASN (P<0.05). Conclusion: We confirmed the great etiological heterogeneity of severe neutropenia in this study. The kinetics of recovery from neutropenia was different between the ASN and CSN group and the complete blood counts may be useful indices for discriminating ASN from CSN. Key Words: Neutropenia, Acute neutropenia, Severe chronic neutropenia pissn -550 / eissn Clin Pediatr Hematol Oncol 04;:59 64 Received on September 0, 04 Revised on October 9, 04 Accepted on October 4, 04 Corresponding Author: Nack-Gyun Chung Department of Pediatrics, Seoul St. Mary s Hospital, The Catholic University of Korea College of Medicine, Banpo-daero, Seocho-gu, Seoul 7-70, Korea Tel: Fax: cngped@catholic.ac.kr 서 호중구감소증은절대호중구수가영아기에 /L 미 론 만, 그이후시기에는 /L 미만인경우로정의한다 [,]. 특히중증호중구감소증은호중구수가 /L 미만인경우로호중구감소증의정도와감염의중증도및빈도는밀접한연관이있는것으로알려져있어임상적으로중요하 59

2 Jin Hee Lee, et al 다. 이러한중증호중구감소증은일과성 ( 또는급성 ) 과만성 ( 또는지속성 ) 으로분류할수있는데만성의기준은보고자에따라 개월또는 6개월이상지속되는경우로정의하고있다 [-6]. 호중구감소증은다양한선천적또는후천적요인에의해발생한다 [7,8]. 소아에서호중구감소증은비교적흔히접하게되는문제이나상당수그원인을알수없는특발성인경우가많고임상경과도매우다양하다. 또한진단및치료에대한지침을임상에직접적용하는것이용이하지않아감별진단을위해많은시간이필요한경우도있고최종원인을알수없는경우도있다 [7,9]. 특히, 국내에서는호중구감소증의임상경과에대한보고가없어호중구감소증이확인된경우임상적인경과관찰과예후예측에대한뚜렷한판단기준이없으며만성호중구감소증의경우개개환자의특성이나임상의의경험에따라치료나추적관찰주기등이결정되고있다. 본연구는감염의위험이높은중증호중구감소증이발생하였던소아청소년에서호중구감소증의예후와회복과관련한지표를확인하고자호중구감소증의발생원인과임상경과를조사분석하였다. 대상및방법가톨릭대학교서울성모병원소아청소년과에서 009년 4월부터 04년 7월까지호중구수가 /L 미만인중증호중구감소증으로진단을받았던환자들을대상으로하였다. 재생불량빈혈과골수부전으로진행하는범혈구감소증의혈액질환, 악성혈액종양질환에의한이차적인호중구감소증은대상에서제외하였다. 의무기록을토대로대상자들의인구학적특징, 병력, 혈액학적소견, 연관감염및임상경과를조사하였다. 호중구감소증이 개월이내에회복된경우를급성중증호 중구감소증 (acute severe neutropenia, ASN) 으로 개월이상지속된경우를만성중증호중구감소증 (chronic severe neutropenia, CSN) 으로분류하여특성을비교하였다. 선천호중구감소증이의심되는 CSN군의 8예는 ELANE (elastase, neutrophil expressed), HAX (HCLS associated protein X-) 유전자변이를검사하였다. 본연구의분석에서중증호중구감소증환자들의구성및특성을살펴보기위해빈도분석 (frequency analysis) 을실시하였으며급성및만성중증호중구감소증의인구통계학적변인과혈액소견에따른차이검증을실시하기위한통계방법으로독립이표본 t-검증 (independent two-samples t-test) 과카이제곱 ( ) 차이검증을실시하였다. 결과조사기간중대상중증호중구감소증환자는총 07예였으며남아가 58예 (54.%) 여아가 49예 (45.8%) 였다. 급성 (ASN 군 ) 이 7예 (67%), 만성 (CSN군) 이 5예 (%) 였으며진단시나이의중앙값은 ASN군이 5.개월로 CSN군의 0.7개월에비하여높았으며 (P=0.004) 두군간성별분포의차이는없었다 (Table ). 호중구수와혈색소수치는 ASN군에비하여 CSN군이유의하게낮았으나전체백혈구수는 CSN군에서오히려높았다. 단구세포수및호산구수및혈소판수도 ASN군에비하여 CSN군에서유의하게높았다 (Table ). ASN군은대부분발열및급성감염으로입원시검사한혈액검사를통해진단이되었으며입원당시임상경과와검사를통한호중구감소증의발생원인으로는감염 54예, 약물 예, 예방접종 예, 불명열 예였고원인추정도불가한경우가 예였다. 감염의원인으로혈청항체나연쇄중합반응으로확 Table. Comparison between patients with acute and chronic severe neutropenia Acute neutropenia n=7, Median (range) Chronic neutropenia n=5, Median (range) P-value Sex male/female Age at onset (months) Hemoglobin (g/dl) White blood cell count ( 0 6 /L) ANC at onset ( 0 6 /L) ANC nadir ( 0 6 /L) Monocyte count ( 0 6 /L) Eosinophil count ( 0 6 /L) Platelet counts ( 0 9 /L) 7 (5%)/5 (48%) 5. (0-6).6 (9.-5.6),99 (,640-8,650) 90 (0-490) 00 (0-490) 50 (-,78) 4 (0-,5) 66 (5-455) (60%)/4 (40%) 0.7 (-). (8.8-4.) 6,980 (,450-4,90) 0 (0-480) 0 (0-80) 79 (09-,64) 66 (0-7) 99 (46-85) <0.00 <0.00 < < Vol., No., October 04

3 Severe Neutropenia in Childhood 인된바이러스감염 4예 (%), 기타호흡기계감염 예 (%), 소화기계감염 4예 (6%), 비뇨기계감염 예 (4%), 피부감염 예가있었다. 확인된바이러스감염은 Parainfluenza 6 예, Coronavirus 4예, Human Herpes virus 6 예, Respiratory Syncytial virus 예, Influenza virus, Metapneumovirus, Hepatitis A virus, Norovirus, Rota virus 가각각 예였다 (Table ). 6예는원인미상의초기발열증상이호전되면서피부발진이생겨돌발진의추정임상진단을받았다. CSN군은처음호중구감소증의진단시임상소견은바이러스감염이 9예 (6%), 호흡기계감염 예 (4%), 비뇨기계및피부감염이각각 예였으며불명열이있었던경우가 예, 전원등의이유로정확한병력확인이어려웠던경우가 6예였다 (Table ). 진단초기에피부감염이있었던 예와전원되어초기병력확인이어려웠던 예, 모두 예에서 ELANE 유전자변이가확인되어선천성호중구감소증이확인되었다 (Table 4). 전원되었던 예는 40회이상의반복적인감염과이에따른합병증의발생등으로비혈연간조혈모세포이식을시행후 Table. Causes of acute severe neutropenia Etiology of neutropenia Number Percentage (%) 양호한상태로경과관찰중이다. ASN군의중증호중구감소증의호전기간은중앙값 7일 ( 범위 -5일 ) 이었다 (Fig. A). CSN군에서는 5예중 예 (60%) 에서호중구감소증에서회복된것을확인할수있었으며 개월이전에회복된경우는 0예, 개월이후에회복된경우는 예였다 ( 범위 4개월-8개월 ). CSN군의 50% 에서호중구감소증이호전되는데까지걸린기간은 8개월이었다 (Fig. B). 고찰선천성호중구감소증은 00만명당 6.명발생으로매우드물고만성호중구감소증의발생도 0만명당.7명정도로드물지만이차성호중구감소증은임상에서비교적흔히접할수있는질환이다 [0,]. 이차성호중구감소증은주로연령이어린소아에서많이발생하는것으로보고되고있으며본조사에서도전체 07예중 97예 (9%) 가 5세이하에서발생하였고특히만성중증호중구감소증의경우모두 개월이전에발생하였다. 호중구감소증은비교적흔히볼수있는골수내골수구계세포에감염, 약물등외인성요인에의해발생할수있으며 Viral infection Parainfluenza Coronavirus Human Herpes virus 6 Respiratory Syncytial virus Influenza virus Metapneumovirus Hepatitis A virus Norovirus Rota virus Other respiratory infection Urogenital infection Gastrointestinal infection Skin infection Drug (anticonvulsant) Vaccine Unknown fever Idiopathic Total Table. Initial presentation of chronic severe neutropenia Initial presentation Number Percentage (%) Viral infection Parainfluenza Respiratory Syncytial virus Adenovirus Rhinovirus Coronavirus Human Herpes virus 6 Influenza virus Other respiratory infection Urogenital infection Skin infection Drug (Immunoglobulin) Unknown fever Not applicable Total Table 4. ELANE mutations in patients with chronic severe neutropenia Case Sex Age Base change Protein change Effect Location Female Male Male 8 year month month c.67-a>t c.60delg c.640g>a p.leu_gln4del p.(asp0thrfs*) p.(gly4arg) Splicing error PTC a) Missense Intron Exon5 Exon5 a) Premature termination codon. NM_0097. and NP_0096. were used to annotate base and protein sequence data, respectively. Clin Pediatr Hematol Oncol 6

4 Jin Hee Lee, et al Fig.. Time duration of recovery from neutropenia. (A) group of acute severe neutropenia (days) and (B) group of chronic severe neutropenia (months). 이보다드문재생불량빈혈및악성혈액질환과같은골수구계세포의후천성질환, 그리고아주드물게발생하는골수구계세포의성숙과증식에내재적이상이있는경우로분류할수있다 [,]. 호중구감소증의주된증상은감염과연관된증상이지만혈액학적검사로확인하기전무증상인경우도있고대부분경한임상증상으로표현되지만입원이필요한중등도이상의감염이반복되어적극적으로항균제나항진균제를투여해야하는경우도있고과립구집락자극인자 (granulcyte colony-stimulating factor, G-CSF) 를투여해야하거나조혈모세포이식을해야하는경우까지다양한임상증상으로표현된다 [6,7,-5]. 소아연령에서발생하는호중구감소증은발열과연관되어발생하는경우가많으며다양한바이러스질환들이연관되어있다고보고되고있다 [4,9,6,7]. 본조사에서총 07예중진단시발열이있었던경우는 ASN군은 7예중 69예 (96%), CSN군은 5예중 0예 (86%) 로중증호중구감소증의초기진단시발열이주된소견임을확인할수있었다. 또한전체증례중 예 (%) 에서진단시바이러스감염이있었음을확인할수있었다. ASN군에서는 Parainfluenza virus, Coronavirus, HHV 6, RSV, Influenza virus, Metapneumovirus 등의연관된바이러스감염을 4예에서확인하였으며이는이전의보고들과같이다양한바이러스감염이호중구감소증의발생과연관이있음을보여주고있다. 특히발열의원인을알수없었던 예에서돌발진을시사하는임상소견을보여급성호중구감소증 55예중감염이원인인 0 예중 9예 (0%) 에서 HHV6가확인된 Husain 등 [6] 의보고와같이바이러스검사를통한확진을하지는못했으나소아에서흔한 HHV 6 감염이호중구감소증과연관이높을가능성을 의심해볼수있었다. CSN군에서도다른보고들과같이진단초기에 ASN군과동일한바이러스들을포함한감염관련원인들이연관되어있음을확인하였다 [4,8]. 호중구감소증이회복되는임상경과를보면 ASN의경우전체 7예중 8예 (5%) 가일주일이내에회복되었으며 0일이내에 65예 (90%) 가회복되었고 5일이내에모두회복되어한달정도의경과관찰을통해회복되지않는경우 개월이상장기간호중구감소증이지속될가능성이높음을알수있었다. CSN군은호중구감소증이호전된 예중 년이내에회복된경우가 0예, 이후에회복된경우가 예였으며 년이후에회복된경우도 예있었다. 따라서 CSN군의경우 년이상회복되지않은증례는 5예 (7%) 로 개월이상지속되는중증호중구감소증의경우 년이상장기간의경과관찰이필요한경우가많은것을알수있었다. 특히다양한감염으로 5회이상입원치료를하였던증례 6명중 예가각각 6개월, 0개월에호전되었으나나머지 4예는각각, 7개월, 7개월, 99개월, 6개월경과관찰중으로반복적인입원치료를요하는호중구감소증의경우좀더장기적인경과관찰이필요함을알수있었다. 이중 예는 ELANE 유전자변이가확인되었으며반복적인감염으로 40회이상의입원치료가수시로필요한상태여서조혈모세포이식을시행하였던증례로진단후 99개월에비혈연간조혈모세포이식후양호한임상경과를보이고있었다. 과거중증호중구감소증환자에서비장적출술, 스테로이드, 면역억제제, 다양한면역글로불린제재등이치료로사용되었으나효과적이지못하였고현재 G-CSF가구강궤양, 발열, 감염관련합병증등의빈도를줄일수있는유용한제재로사용 6 Vol., No., October 04

5 Severe Neutropenia in Childhood 되고있다 [6]. 그러나 G-CSF는골수형성이상증후군또는골수성백혈병으로이행시킬위험성에대한논란이있어정상범위의중성구수를유지하기보다는정상적인삶을영위하는데필요한최소량을주는것이원칙이다 [,9-]. 본조사에서도 CSN 군에서발열등감염증상의호전을목적으로 G-CSF 를사용하였던경우는 예 (%) 였으며 G-CSF를사용한경우모두호중구감소증이회복되면서관련임상증상이호전되는것을확인할수있었다. 전체적인추적관찰기간이짧기는하지만연구대상자중골수형성이상증후군이나골수성백혈병으로진행된증례는없었다. 일반적으로호중구감소증이지속되는경우라도말초에서중성구와같이대식구와같은식세포기능을가지고있는단구가증가되면감염에대한저항성이증가되고임상양상이양호한것으로알려져있다. 반응성혈소판증가증의경우그원인은정확하게알수없으나골수에서지속되는감염상태나염증상태에서 thrombopoietin, interleukin-6 및다른싸이토카인들이분비되어다른계열의세포들이증가하는것으로추정하고있다 []. 본조사에서는호중구감소증이 개월이상지속하는 CSN군의경우 ASN 군에비해혈소판수가유의하게높은것을확인할수있었다. 만성중증호중구감소증의경우단구의증가, 혈소판증가와약간의빈혈이있는것을특징으로한다고하며 [4], 본연구에서도 CSN군에서이와일치하게단구및혈소판수가 ASN군보다높고혈색소수준은낮은것을확인할수있었다. Sheen 등은이차성호중구감소증이있는환자들을대상으로만성경과를밟을수있는위험인자로중증호중구감소증이외에연령 세미만, 혈소판수증가및거대세포바이러스감염을보고하여본연구의 ASN군과비교한 CSN군에서의연령과혈소판수의특성과일치하고있었다 [8]. 현재까지알려진중증만성호중구감소증의분자유전학적진단중가장흔한유전자적이상은 ELANE 과 HAX 유전자변이이다 [5-7]. 본조사에서만성중증호중구감소증의원인을확인하기위하여 ELANE 및 HAX 유전자변이를검사한경우는모두 8예였으며이중 예에서 ELANE 유전자변이를확인하였다. 이들중 예에서는출생 개월이내에피부감염을동반한발열의병력이있었고다수의입원병력을보이고있어이러한경과를보이는만성중증호중구감소증의경우적극적으로유전자검사등을통한감별진단이필요할것으로판단된다. 그러나아직국내에서다양한질환에대한유전자검사체계가갖추어져있지않고아직밝혀지지않은유전적요인들도많을것으로추정되어만성경과의중중호중구감소증의진단에어려움이있을것으로예상된다. 본연구는중증호중구감소증을보였던환자대상으로후향적으로자료를수집한연구로단일기관의연구이므로호중구감소증의전체적인빈도등을확인할수는없었으며실제중증호중구감소증이있었던증례들도모두조사되지않았을가능성도있는것이제한점이라하겠다. 그러나대상군의일반적인특성은확인할수있었으며비교적많은증례들이초기발열증상및다양한감염추정증상및확인된원인으로중증호중구감소증이발생함을확인할수있었다. 또한만성경과를보이는경우발생연령이낮았으며백혈구, 단구, 호산구, 혈소판수가만성인경우에서급성보다높은것을확인할수있어연령과혈액학적소견이회복시기를예측하는지표로참고가될수있음을확인하였다. 감사의글 This study was supported by a grant of the Korea Health technology R&D Project, Ministry of Health & Welfare, Republic of Korea (A075). 참고문헌. Segel GB, Halterman JS. Neutropenia in pediatric practice. Pediatr Rev 008;9:-.. Haddy TB, Rana SR, Castro O. Benign ethnic neutropenia: what is a normal absolute neutrophil count? J Lab Clin Med 999;:5-.. Dale DC, Bolyard AA, Schwinzer BG, et al. The Severe Chronic Neutropenia International Registry: 0-Year Follow-up Report. Support Cancer Ther 006;: Karavanaki K, Polychronopoulou S, Giannaki M, et al. Transient and chronic neutropenias detected in children with different viral and bacterial infections. Acta Paediatr 006;95: Bernini JC. Diagnosis and management of chronic neutropenia during childhood. Pediatr Clin North Am 996;4: Dale DC, Cottle TE, Fier CJ, et al. Severe chronic neutropenia: treatment and follow-up of patients in the Severe Chronic Neutropenia International Registry. Am J Hematol 00;7: Fioredda F, Calvillo M, Bonanomi S, et al. Congenital and acquired neutropenia consensus guidelines on diagnosis from the Neutropenia Committee of the Marrow Failure Syndrome Group of the AIEOP (Associazione Italiana Emato-Oncologia Pediatrica). Pediatr Blood Cancer 0;57: Boxer LA. How to approach neutropenia. Hematology Am Soc Hematol Educ Program 0;0:74-8. Clin Pediatr Hematol Oncol 6

6 Jin Hee Lee, et al 9. Angelino G, Caruso R, D'Argenio P, et al. Etiology, clinical outcome, and laboratory features in children with neutropenia: analysis of 04 cases. Pediatr Allergy Immunol 04; 5: Donadieu J, Fenneteau O, Beaupain B, Mahlaoui N, Chantelot CB. Congenital neutropenia: diagnosis, molecular bases and patient management. Orphanet J Rare Dis 0;6:6.. Rajantie J, Kurki S, Juvonen E, Hovi L. Prolonged pure granulocytopenia in children. Acta Paediatr 99;8: Newburger PE, Boxer LA. Leukopenia. In: Kliegman RM, Stanton B, Geme J St., Schor N, Behrman RE, editors. Nelson textbook of pediatrics. 9th ed. Philadelphia: Elsevier Saunders, 0; Newburger PE, Dale DC. Evaluation and management of patients with isolated neutropenia. Semin Hematol 0;50: Vlacha V, Feketea G. The clinical significance of non-malignant neutropenia in hospitalized children. Ann Hematol 007; 86: Wan C, Yu HH, Lu MY, et al. Clinical manifestations and outcomes of pediatric chronic neutropenia. J Formos Med Assoc 0;: Husain EH, Mullah-Ali A, Al-Sharidah S, Azab AF, Adekile A. Infectious etiologies of transient neutropenia in previously healthy children. Pediatr Infect Dis J 0;: Alexandropoulou O, Kossiva L, Haliotis F, et al. Transient neutropenia in children with febrile illness and associated infectious agents: years' follow-up. Eur J Pediatr 0;7: Sheen JM, Kuo HC, Yu HR, Huang EY, Wu CC, Yang KD. Prolonged acquired neutropenia in children. Pediatr Blood Cancer 009;5: Dale DC, Bonilla MA, Davis MW, et al. A randomized controlled phase III trial of recombinant human granulocyte colony-stimulating factor (filgrastim) for treatment of severe chronic neutropenia. Blood 99;8: Rosenberg PS, Zeidler C, Bolyard AA, et al. Stable long-term risk of leukaemia in patients with severe congenital neutropenia maintained on G-CSF therapy. Br J Haematol 00; 50: Rosenberg PS, Alter BP, Bolyard AA, et al. The incidence of leukemia and mortality from sepsis in patients with severe congenital neutropenia receiving long-term G-CSF therapy. Blood 006;07: Yoo ES. Neutropenia in children. Korean J Pediatr 009;5: Dame C, Sutor AH. Primary and secondary thrombocytosis in childhood. Br J Haematol 005;9: Boxer L, Dale DC. Neutropenia: causes and consequences. Semin Hematol 00;9: Ancliff PJ, Gale RE, Liesner R, Hann IM, Linch DC. Mutations in the ELA gene encoding neutrophil elastase are present in most patients with sporadic severe congenital neutropenia but only in some patients with the familial form of the disease. Blood 00;98: Klein C, Grudzien M, Appaswamy G, et al. HAX deficiency causes autosomal recessive severe congenital neutropenia (Kostmann disease). Nat Genet 007;9: Ward AC, Dale DC. Genetic and molecular diagnosis of severe congenital neutropenia. Curr Opin Hematol 009;6: Vol., No., October 04

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