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Acta Cirurgica Brasileira

Print version ISSN 0102-8650On-line version ISSN 1678-2674

Acta Cir. Bras. vol.14 n.3 São Paulo Sept. 1999

http://dx.doi.org/10.1590/S0102-86501999000300006 

Bone mineral density in children and adolescents with hepatosplenic mansonic schistosomiasis and esophageal varices who underwent splenectomy and ligature of the left gastric vein1

 

Carlos Teixeira Brandt2
Antonio Marcelo Gonçalves de Souza3
Maria Virgínia da Motta Braga4
Karina Leal Reis de Melo4
Fernando Almeida5

 

 

Brandt CT, Souza AMG, Braga MVM, Melo KLR, Almeida F. Bone mineral density in children with hepatosplenic mansonic schistosomiasis and esophageal varices who underwent splenectomy and ligature of the left gastric vein. Acta Cir Bras [serial online] 1999 Jul-Sept;14(3). Available from: URL: http://www.scielo.br/acb .

SUMMARY: Twenty eight children and adolescents from 7 to 19 years of age, suffering from hepatosplenic mansonic schistosomiasis and bleeding esophageal varices were evaluated for bone mineral density (BMD), before undergoing medical and surgical treatment. The surgical protocol was splenectomy, autoimplantation of spleen tissue into a pouch of the greater omentum and ligature of the left gastric vein. Twenty one patients were evaluated after a follow up from two to nine years post surgical treatment. The BMD was measured at the lumbar spine (L2 – L4) through the dual energy absorptionmetry X-ray (DEXA), using a LUNAR DPX-L densitometer. Preoperatively, all patients showed deficit of the BMD varying from 1 to 7.07 standard deviations (Mean ± SEM – 2.64 ± 0.28), considering the mean line of the control curve for healthy children accepted as normal. The BMD deficit was more evident among the females than the males. After treatment there was a significant increment (C2 = 9.19 – p =0.01) of the BMD and 29% of the patients (six out of twenty one) were considered without bone mineral deficit. It was concluded that the patients included in this series, who suffer from hepatosplenic mansonic schistosomiasis, showed an important BMD deficit, specially among the females which has had a significant improvement after medical and surgical treatment.
SUBJECT HEADINGS: Schistosomiasis mansoni. Hypertension, portal. Splenectomy. Bone density.

 

 

INTRODUCTION

Apart from recurrent upper digestive hemorrhage, hepatosplenic mansonic schistosomiasis, in children shows several other clinical manifestations including hipersplenism, developmental deficit and bone age retardation1,2,3. The routine investigation for bone age in these children has been done by wrist X-ray using the Greulich and Pyle scale as a normal reference. This technique is merely comparative with low precision.

Bone mineral density (BMD) has been considered the best way of measuring mineral content of the bone tissue. It implies a high diagnostic precision with a mean standard deviation of 1.3%4,5. The main indications for assessing the BMD in children are for those with diseases which interfere with the vitamin D metabolism and hepatic functional reserve. It also has been used in children suffering from chronic nephropathy which can produce secondary hyperparathyroidism and consequent changes in the bone metabolism5. Other indications include intestinal malabsorption and imperfect osteogenesis.

Since January 1990 the Unit of Pediatric Surgery in The University Hospital – Federal University of Pernambuco has been treating children suffering from hepatosplenic mansonic schistosomiasis and bleeding esophageal varices with splenectomy, ligature of the left gastric vein and autologous implantation of spleen tissue into an omental pouch of the greater omentum. Endoscopic sclerosis for the esophageal varices has been used postoperatively in the patients with recurrent bleeding from these varices. It has been shown that the patients in this series, although decreasing the portal blood inflow and increasing the hepatic arterial inflow, they are maintaining their hepatic functional reserve and they are improving their development. With this surgical approach it has been avoided increase in the rate of infections and there has been no case of overwhelming post splenectomy sepsis,6,7,8.

It has been reported that patients with liver fibrosis and ascites due to schistosomiasis develop a significant hypocalcaemia, hypomagnesaemia and hyperphosphataemia. These metabolic changes may be associated with excess in aldosterone secretion, combined with hypoparathyroidism9. Taking into account that the patients with hepatosplenic mansonic schistosoniasis come from a population with low intake in proteins and vitamins it is foreseeable that they have alterations in their bone health.

The aim of this investigation was, prospectively, to evaluate the BMD of children with hepatosplenic mansonic schistosomiasis and bleeding esophageal varices who were treated with oxamniquine and underwent splenectomy, ligature of the left gastric vein and autologous implantation of spleen tissue into the greater omentum.

 

METHOD

Twenty eight children and adolescents from 7 to 19 years of age, at the time of surgical treatment, 16 males and 12 females, suffering from hepatosplenic mansonic schistosomiasis and bleeding esophageal varices with or without hypersplenism and developmental retardation were included in this investigation.

The Child’s criteria for assessment of hepatic functional reserve were used. In addition the prothrombin time was also assessed. Before surgical treatment nine were classified in grade A (good risk) and nineteen in grade B (moderate risk) of the Child’s criteria for hepatic functional reserve. Liver function test for hepatits B antigenemia were done in all patients.

As regard to their somatic development they were compared with the standard curve for the brazilian normal population. Sixteen patients (57%) were under the percentile 2.5, ten (36%) were between the percentiles 2.5 and 25 and two (7%) were between the percentiles 25 and 75. For regional control group of this parameter, 57 children, 39 males and 18 females, aged 5 to 15 years, coming from the same environment with similar social and economical conditions, without schistosomiasis, were assessed for somatic development. Using the same standard curve, two (3%) of these children and adolescents were under the percentile 2.5, twenty one (37%) were between the percentiles 2.5 and 25, twenty four (42%) were between percentiles 26 and 75, eight (14%) were between the percentiles 76 and 97.5 and two (3%) were over the percentile 97.5. From this control group 15 males and 10 females were assessed for bone mineral content. Using the standard curve for the healthy Spanish population, 12 (48%) of these children and adolescents were considered normal, 10 (40%) osteopenic and 3 (12%) suffering from osteoporosis.

The patients with hepatosplenic mansonic schistosomiasis were evaluated for bone mineral density (BMD), before receiving medical treatment with oxaminquine 20mg/Kg and undergoing splenectomy, ligature of the left gastric vein and autologous implantation of approximately 100g of spleen tissue into an omental pouch of the greater omentum. Liver biopsy from all patients was sent for histophatology.

After a postoperative follow-up from two to nine years (average four years) the BMD was measured again in twenty one patients.

The BMD was measured at the lumbar spine (L2 – L4) through the dual energy absorptionmetry X-ray (DEXA), using a LUNAR DPX-L densitometer. The BMD was considered normal until 0.99 Standard Deviation (SD) considering the mean line of the control curve for healthy children accepted as normal. Osteopenia was considered when the deficit was between 1.0 and 2.5 SD of this mean line while osteoporosis was considered when the mineral density deficit was greater than 2.5 SD.

 

RESULTS

The BMD results of the patients with hepatosplenic mansonic schistosomiasis before and after medical and surgical treatment are expressed in graphic representations (Figures 1,2,3 and 4) and Tables 1,2 and 3.

 

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Figure 1 - Pre-operative values of BMD in males.

 

 

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Figure 2 - Pre-operative values of BMD in females.

 

 

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Figure 3 - Post-operative values of BMD in males.

 

 

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Figure 4 - Post-operative values of BMD in females.

 

 

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3a06t2.gif (3884 bytes)

 

 

3a06t3.gif (3873 bytes)

 

DISCUSSION

As compared to the regional control group the children with hepatosplenic mansonic schistosomiasis and bleeding esophageal varices showed a significant retardation in their somatic development, either related to the body weight (X2 = 33.4 p<0.001) and height (X2 = 36.7 p<0.001). The distribution of body weight and height of both groups are concentrate in the lower percentiles of the standard curve, for these parameters, of the normal Brazilian population. As regard to bone mineral density the findings also showed a significant decrease of the mineral content in the group of patients as compared with the regional control group (X2 = 17.9 p<0.001). It makes evident that all these children suffer from malnutrition. These findings, however, stress that the endemic schistosomiasis aggravates the nutritional status of the children with this disease in northeast – Brazil.

As it would be expected, in children with chronic liver disease, the results confirm the deficit in the bone mineral content of the patients included in this investigation. The BMD of all patients were under the inferior limit of the mean value of the normal curve. It is noticed that four female patients were well below the BMD of the male patients. It is likely that because puberty in females is earlier than in males and it is associated with a greater increment in the bone mineral content, the changes in the bones of the females at adolescence would be more important than in males.

The findings of increment in the bone mineral content in adolescents with hepatosplenic mansonic schistosomiasis after splenectomy are, in some way, similar to those previous reported using the bone age. However, the comparison of the wrist X-ray with the Greulich and Pyle scale reveal a reliability of 60% while the precision of the BMD is close to 100%, with a standard deviation of 0.01g/cm2. On the other hand, the higher survival rate of the patients in this series has allowed a greater follow-up than in the past series when spleen tissue auto-implantation was not done and the mortality rate was too high. This increment, after medical and surgical treatments, of the bone mineral content, in the adolescents included in this investigation may reflect the maintenance, or even slight improvement of the hepatic functional reserve7.

The six patients who have still osteoporosis are among the ones with moderate risk (B) in the Child classification for hepatic functional reserve and they have lower prothrombin time than the patients with A in the Child classification who have either osteopenia or normal bone mineral content. Five of the them ( 83%) showed Symmers fibrosis grade III and one grade II on liver histopathology Furthermore cirrhotic changes was evident in two of these patients, both with positive hepatitis B antigenemia.

The six patients with normal bone mineral content at follow up are all included as Child A for hepatic functional reserve, all had Symmers fibrosis grade I and all has been showing normal prothrombin times.

It seems likely that bone mineral content may reflect, among other metabolic changes, the severity of the hepatic disease and the consequent status of liver function of the patients included in this series.

It is well known that there are, in the liver and kidney, several biochemical reactions which convert vitamin D3 in its final and active product (25 – dihydroxicalciferol). This metabolic step is essential for the absorption of the calcium from the gut to the plasma and the bone5. Furthermore, it has been suggested that magnesium depletion is common in children with chronic hepatic disease and this deficiency may alters vitamin D metabolism by decreasing parathyroid hormone response, resulting in decreasing osteocalcin and decreased bone accretion10. In cirrhotic patients referred for orthotopic liver transplantation severe osteoporosis and bone mineral metabolism disorders are associated with low serum levels of 25-hydroxyvitamin D, 1,25-dihydroxyvitamin D and parathyroid hormone11. On the other hand, it is also common in patients with chronic liver disease specially in schistosomotic the association with glomerular disease12,13,14. This association may cause secondary hyperparathyroidism which could also be implicated in the bone mineral content changes.

 

REFERENCES

1. Silveira GK. Efeito da esplenectomia sobre o hormônio do crescimento em pacientes portadores de esquistossomose mansônica hepatoesplênica e hipodesenvolvimento somático [tese Mestrado] Recife: Universidade Federal de Pernambuco; 1976.        [ Links ]

2. Brandt CT, Tavares DJS. Esplenose associada a esplenectomia em crianças esquistossomóticas: análise seqüencial das imunoglobulinas G, A e M e dos componentes 3 e 4 do sistema complemento. An Fac Med Cent Ciênc Saúde/UFPE 1993;38:24-9.        [ Links ]

3. Domingues ALC, Domingues LAW. Forma intestinal, hepatointestinal e hepato-esplênica. In: Malta J. Esquistossomose mansônica. Recife: Editora Universitária da UFPE; 1994. p. 91-109.         [ Links ]

4. Souza AMG, Brandt CT, Almeida F. Densidade mineral óssea (BMD) em crianças esquistossomóticas na forma hepatoesplênica com indicação cirúrgica. An Fac Med Cent Ciênc Saúde/UFPE 1993;38(2):9-11.         [ Links ]

5. Pons F, Del Rio L. Aplication de los estudios densitométricos en pediatria. Rev Esp Med Nuclear 1991; 10:65-7.        [ Links ]

6. Brandt CT, Frei Caneca OA, Tavares, DJS, Ávila JR. Surgical hepatosplenic mansonic schistosomiasis in children: a Doppler Duplex study of the portal vein and hepatic artery. Trans R Soc Trop Med Hyg 1995;89:70-1.        [ Links ]

7. Brandt CT, Tavares Maciel DS, Caneca OAF. Splenectomy associated with ligature of the left gastric vein in children with schistosomiasis: analysis of the hepatic functional reserve. Acta Cir Bras 1997;12: 150-3.         [ Links ]

8. Brandt CT, Araujo LB, Barbosa CM. Autotransplantation of spleen tissue in children with mansonic schistosomiasis who underwent splenectomy: evaluation of splenic residual functions. Acta Cir Bras 1998;13:212-6.        [ Links ]

9. Hathout S M, El-Karim AH, El-Masry AA. Serum calcium, magnesium and phosphate in bilharzial hepatic fibrosis. Egypt J Bilharz 1979;6:25-30.        [ Links ]

10. Heubi JE, Higgins JB, Argao E A, Sierra RI, Specker BL. The role of magnesium in the pathogenesis of bone disease in childhood cholestatic liver disease: a preliminary report. J Pediatr Gastroenterol Nutr 1997;25:301-6.        [ Links ]

11. Monegal A, Navasa M, Guanabens N, Peris P, Pons F, Martinez de Osaba MJ, Rimola A, Rodes J, Munoz-Gomez J. Ossteoporosis and bone mineral metabolism disorders in cirrhotic patients referred for orthotopic liver transplantation. Calcif Tissue Int 1997;60:148-54.         [ Links ]

12. Andrade ZA, Vanmarck E. Schistosomal glomerular disease (a review). Mem Inst Oswaldo Cruz 1984;79:499-506.        [ Links ]

13. Chugh KS, Sakhuja V. Glomerular diseases in the tropics. Am J Nephrol 1990;10:437-50.        [ Links ]

14. Barsoum RS. Schistosomal glomerulopaties. Kidney Int 1993;44:1-12.         [ Links ]

 

 

Brandt CT, Souza AMG, Braga MVM, Melo KLR, Almeida F. Densidade mineral óssea em crianças portadoras de esquistossomose hepatoesplênica e varizes esofageanas que se submeteram a esplenectomia e ligadura da veia gástrica esquerda. Acta Cir Brás [serial online] 1999 Jul-Set;14(3). Available from: URL: http://www.scielo.br/acb .

RESUMO: Vinte e oito crianças e adolescentes de 7 a 19 anos, portadoras de hepatoesplenomegalia esquistossomótica e varizes sangrantes do esôfago foram avaliadas quanto ao conteúdo mineral ósseo (BMD), antes de serem submetidas a tratamento clínico e cirúrgico. O protocolo cirúrgico consistia de esplenectomia, auto-implante esplênico no omento maior e ligadura da veia gástrica esquerda. Vinte e um pacientes foram avaliados após seguimento pós-operatório de dois a nove anos. O BMD foi medido nas vértebras lombares (L2 – L4) através do método de "Dual energy absorptionmetry X-ray (DEXA)", usando um densitômetro LUNAR DPX-L. No pré-operatório todos os pacientes evidenciavam déficit do BMD variando de 1 a 7,07 desvios padrão (Média ± Erro Padrão da Média – 2,64 ± 0,28), considerando a linha média da curva de controle para os indivíduos sadios aceitos como normais. O déficit de BMD foi maior nas pacientes do sexo feminino do que as do sexo masculino. Após tratamento, houve um incremento significativo ( C 2 = 9,19 – p =0,01 ) do BMD e 29% dos pacientes (seis em vinte e um) foram considerados sem déficit do conteúdo mineral ósseo. Pode-se concluir que os pacientes incluídos nesta série, que sofriam de esquistossomose mansônica hepatoesplênica evidenciavam um importante déficit do BMD, especialmente entre as pacientes do sexo feminino, os quais tiveram uma melhora significativa após tratamento clínico e cirúrgico.
DESCRITORES: Esquistossomose mansoni. Hipertensão portal. Esplenectomia. Auto-implante esplênico. Densidade óssea.

 

 

 

Address for correspondence:
Carlos Teixeira Brandt
R. 19 de Abril, 30/602
52071-332 – Recife-PE

Data do recebimento: 08/03/99
Data da revisão: 05/04/99
Data da aprovação: 10/05/99

 

 

 

1 Work from Pediatric Surgical Service of the University Hospital, Pernambuco – Brazil
2 Head Professor of Pediatric Surgery – Federal University of Pernambuco – Brazil
3 Assistant Professor of Orthopedic Surgery - Federal University of Pernambuco – Brazil
4 Medical Students (CNPq Grant) - Federal University of Pernambuco – Brazil
5 Medical Specialist in Nuclear Medicine

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