Cord Blood Transplantation: Early Work. Hallmarks of the 20th Century

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1 C O R D B L O O D T R A N S P L A N T S Virginia C. Hughes, MS, MT(ASCP) Cord Blood Transplantation: Hallmarks of the 20th Century ABSTRACT Significant advances have been made in cord blood research and transplantation in the 20th century. More than 1,000 cord blood transplants have been performed worldwide, successfully treating disorders such as Fanconi anemia, chronic myelogenous leukemia, acute lymphoblastic leukemia, neuroblastoma, Gaucher disease, and hemoglobinopathies (after treatment with chemotherapy). Cord blood transplants have been successful with either matched or mismatched HLAs. Cord blood transplants are successful because they are a rich source of viable stem cells, have minimal maternal T-cell contamination from collection techniques, and their immunologically naive T cells are less likely to invoke a graft-vs-host reaction. This article will highlight strides in cord blood research, including cord blood banking, transplantation, and gene therapy. From the College of Health Sciences, School of Health and Human Services, University of Wyoming, Laramie. Reprint requests to Ms Hughes, College of Health Sciences, Medical Technology Program, University of Wyoming, PO Box 3837, Laramie, WY , or Background Human umbilical cord blood is a rich source of stem cells that are present in bone marrow and that have been used successfully to treat a variety of hematologic diseases. Stem cells divide to make new RBCs, WBCs, and platelets. In persons with hematologic disease, stem cells in cord blood restore marrow function after chemotherapy. To date, more than 1,000 cord blood transplants have been performed worldwide from both HLAmatched and HLA-mismatched donors. The success of these transplants has been attributed to the following factors: maternal T-cell contamination is below the level of detection by DNA techniques, microbial contamination occurs with low frequency with current collection methods, and cord blood contains pluripotent hematopoietic stem cells. Also, an infant s immune system is naive (containing reduced levels of activated T cells) and therefore is less likely to invoke a graft-vs-host rejection. This article serves to identify progress made in the 20th century in cord blood transplants, cord blood banking, and gene therapy. Cord Blood Transplantation: Early Work The concept of umbilical cord blood transplantation was introduced by 2 American brother physicians, Milton and Norman Ende, in The case (published in ) involved a 48-year-old woman diagnosed with lymphangiosarcoma, a malignant tumor of lymphatic vessels arising in a limb that is the site of chronic lymphedema. The disease manifested with recurring cellulitis and edema in the left arm. Treatment for this patient included a forequarter amputation, x-ray, and nitrogen mustard chemotherapy. When lesions reappeared on the extremity and proceeded to infiltrate the left lung, the physicians decided to try a form of therapy never envisioned before: umbilical cord blood transplantation. They had nothing left to try in treatment of this patient. At the time, of course, it was not known that placental blood contains stem cells. In his 1966 paper describing lymphangiosarcoma, Milton Ende revealed that in 1959, Dr. H.T. Schreus in Germany described youth factors that he thought inhibited the appearance of melanosarcomas. He took blood from young children and transfused it to adults. So Milton Ende began giving cord blood randomly for advanced malignant disease in 1961 to see if it had a therapeutic effect

2 In July 1963, blood was collected from the placenta immediately after birth and crossmatched with the patient s blood. A total of 577 ml was transfused in aliquots (ranging from 10 to 52 ml) over a period of 17 days. Although the lesions on the chest wall failed to demonstrate any reduction in size, the patient appeared to feel better, and she was discharged. Several weeks passed; the patient s condition began to worsen. Additional therapy was started, which included chlorambucil, steroids, and repetitive thoracenteses. However, the patient s condition declined rapidly, and she died in March The 1966 article does not give details on how the mothers were chosen only that coordination among the obstetrics department, the laboratory and the attending physicians was necessary. At that time, internal review boards were not as restrictive as they are today. The next recorded transplant using fetal blood was done in 1966 in a patient with myelogenous leukemia. 2 The patient was given approximately 500 ml of cord blood. Samples of the patient s blood were subsequently collected and sent to the Ortho Research Foundation (Raritan, NJ) for serologic testing. Studies revealed that the only cells that had survived were those of the fetal blood transplant. This finding is consistent with hematopoietic reconstitution, where stem cells present in the fetal blood transplant will continuously self-replicate and produce cells comprising the leukocyte, erythrocyte, and platelet lineages, in essence, replacing the abnormal cells of the recipient. Another cord blood transplant was done in 1968 on a patient diagnosed with acute granulocytic leukemia. 2 The patient was given 1 pint of cord blood over a period of 20 days. The physicians noted changes in the Duffy (Fy a ) and S antigens from the pretransplant and posttransplant specimens, suggesting that successful engraftment had taken place. The patient survived for more than 8 months with chemotherapy. The next cord blood transplant occurred in February That case involved a 16-year-old boy diagnosed with acute lymphoblastic leukemia. The patient presented with leukocytosis, anemia, splenomegaly, and marked cervical adenopathy. Treatment was initiated with 6-mercaptopurine and prednisone daily. Fetal blood transfusions were begun on the third day of hospitalization, and the patient received a total of 500 ml over a period of 17 days. As a result of this treatment, the patient s condition improved to near-normal WBC counts and increases in his hemoglobin level. After continued treatments with steroids and chemotherapeutic agents, the patient s blood cell counts reached normal levels. Still later, in 1972, a patient diagnosed with aplastic anemia was given a cord blood transplant. 2 In this particular case, HLA testing did not change between pre-transplant and posttransplant periods; the patient survived 2 years before dying of miliary tuberculosis. Cord Blood Transplantation: Later Work Despite the strides made in the 1960s and the 1970s, the next cord blood transplant did not occur until 16 years later, in A 5-year old boy was transfused with cord blood from his HLAmatched sibling. 4 The patient was diagnosed with Fanconi anemia, a congenital form of aplastic anemia. The ABO and Rh of the donor was O positive; the patient was B-positive. After collection of the umbilical cord blood, the sample was cryopreserved until infused into the patient in October Successful engraftment was evident when the patient s B positive cells were no longer detected on day 90 after transplantation. The patient s bone marrow showed normal cellularity at posttransplant day 120. The first known successful HLA-mismatched cord blood transplant was performed in 1989 in a 2-year old boy with advanced acute lymphoblastic leukemia. 5 The cord blood donation was 80 ml via needle aspiration from his sister. The cord blood was frozen in media without any further manipulation, and HLA compatibility was determined. The donor was mismatched for 1 HLA-A antigen and 1 HLA-DR antigen that the recipient lacked. Section 4 Scientific Communications DECEMBER 2000 VOLUME 31, NUMBER 12 LABORATORY MEDICINE 6 7 3

3 HLA-A is the human leukocyte antigen that encodes for class I major histocompatibility antigens, and HLA(DR) encodes for class II major histocompatibility antigens. Matches between the donor and the recipient yield more successful transplant outcomes. Before transplantation, the patient received total body irradiation as well as prophylaxis to protect against graft-vs-host disease (GVHD). Hematopoietic recovery was satisfied by posttransplantation day 32 with minimal effects of GVHD. HLA typing confirmed the presence of only donor lymphocytes on posttransplantation days 90 and 180. Later mismatched transplants were done in Four patients diagnosed with advanced solid tumors were given HLA-mismatched multiple cord blood transplants, following myelosuppressive chemotherapy. 6 The patients ranged in age from 4 to 11 years, with diagnoses of mucous liposarcoma, neuroblastoma (stage IV), non- Hodgkin lymphoma (stage IV), and yolk sac sarcoma (stage III). Three of 4 patients achieved complete remission, which was defined as the disappearance of tumor according to all indices and survival to at least 30 days after transfusion of cord blood. Mild GVHD was detected in 1 patient. Treatment of thalassemia major in a 3-year-old girl was done in June (Thalassemia is an inherited hematologic disease characterized by increased hemoglobin F, decreased or absent hemoglobin A, microcytic/hypochromic anemia, and organ damage caused by iron overload from frequent blood transfusions.) A cord blood transplant of 44 ml was transfused from her HLAidentical brother 7 (after chemotherapy). This transplant was successful, as evidenced by normal levels of hemoglobin F and hemoglobin A, normal blood counts, and the presence of a male sex chromosome posttransplantation day 373. In December 1998, the first cord blood transplant was performed in a patient with sickle cell anemia. 8 (Sickle cell anemia is an inherited blood disease caused by an amino acid substitution in the hemoglobin molecule, making sickle-shaped RBCs destined for destruction in the spleen.) Seriously ill all his life, the 13-year-old patient decided for himself that this was his last hope. He was given a cord blood transplant from the New York Blood Center, after 9 days of chemotherapy to kill diseased cells in his bone marrow. A year after the transplant, his physicians reported that the cord blood stem cells had engrafted and that all blood counts were normal. Cord Blood Banking Collection of umbilical cord blood normally involves informed consent of the mother and cannulation of the umbilical vein once it has been clamped. Blood is collected into sterile collection bags containing anticoagulants ACD (acid citrate dextrose) or CPD (citrate phosphate dextrose). Volume of cord blood may range from 60 ml to 150 ml. A small volume of cord blood is reserved for HLA typing and stem cell assays, and the remainder is frozen in a cryoprotectant medium for future transplantation. The pioneer of cord blood banking is David Harris, PhD, professor of microbiology and immunology at the University of Arizona, Tucson. His laboratory began collecting and storing cord blood as part of a pilot program with the American Cancer Society in The first sample collected was that of his son. In 1995 he joined with the Cord Blood Registry (CBR) (San Bruno, CA) to create the largest cord blood family bank in the United States. Today he serves as the scientific and laboratory director in that organization. The CBR has collected more than 17,000 cord blood samples to date at more than 1,900 hospitals and birthing centers throughout the United States and in 22 other countries. Additionally, the CBR was the first cord bank to be accredited by the American Association of Blood Banks. The New York Blood Center also established its Placental Blood Program in Its mission was to provide allogeneic (unrelated) cord blood for those patients in need of a transplant for whom a related match could not be found. From 1992 to 1998 the center performed more than 560 unrelated transplants. The study involved nearly 100 transplant centers around the world and the collection of 7,705 units. 11 Eighty-two percent of the patients were younger than 18 years of age, with diseases ranging from acute and chronic leukemias to lipid storage disorders. Myeloid 6 7 4

4 engraftment was evident in 72% of cases defined as having an absolute neutrophil count of 500/µL ( /L; reference range, 4,500-11,000/µL [ /L]) on 3 consecutive days. With engraftment occurring in cord transplants with as many as 2 HLA mismatches, researchers concluded that cord blood transplants involving unrelated donors should be supported. The San Diego Blood Bank was founded in 1998 and named its donor program after an 8- year-old girl diagnosed with Fanconi anemia. 12 Ashley Ross was the first person in San Diego to receive a cord blood transplant, and today, she is disease free. The Ashley Ross Cord Blood Donor Program held the first Cord Blood Drive in 1998 at the San Diego Chargers Blood Drive XX. Expectant mothers in their 36th week of pregnancy received a free collection kit to take to delivery, while other attendees were given information on stem cells and cord blood collection. To date, more than 1,000 cord blood donations have been collected and stored through this program. Internationally, cord blood banks have been established in Great Britain, Italy, Germany, Switzerland, France, the Netherlands, Poland, and Japan. The EUROCORD group was started in 1996 and comprises more than 50 blood centers throughout Europe. 13 The objectives of EURO- CORD are as follows: To standardize the methods of collection, testing, and cryopreservation of cord blood, To study the properties of hematopoietic progenitors and gene transfer in cord blood, To study the immune function of cord blood lymphocytes, To coordinate and facilitate the exchange of sera and cells from donors and recipients of cord blood transplants, To establish a European registry of patients treated with cord blood transplants, To design protocols comparing cord blood transplants with alternative conventional blood and bone marrow transplants. As of 1997, more than 10,000 units of cord blood were available worldwide, according to the Second EUROCORD Transplant Workshop held in that year. (Unfortunately, more a recent count is not available because no third workshop followed.) In an attempt to access available cord blood units in Spain, Germany, and Italy, NETCORD began its program in Each cord blood bank that participates in NET- CORD makes its own inventory accessible online to other cord blood banks, thus facilitating search requests in the hope of expediting transplantations. Gene Therapy The basis of gene therapy involving hematopoietic cells is to transfer new genetic information into stem cells and progenitor cells. The addition of a normal gene to cells exhibiting altered genes is to reverse the phenotype and correct the genetic defect. In cases where a deteriorating disease is detected in a fetus before birth, the abnormal cell pool could realistically be removed by percutaneous umbilical blood sampling or cordocentesis. The cell pool could then be treated with gene therapy and reinfused by ultrasound guidance and intraperitoneal injection. 15 Alternatively, cord blood could be collected at birth, the target cells isolated and inserted with a healthy gene, and the blood reinfused as normal fetal cells. Though there are more than 3,000 genetic diseases known, not all disorders can be treated with gene therapy (Table 1). Table 1. Criteria for Gene Therapy 15 The affected gene must be clonable by DNA techniques. The normal function of the cell should not require precise regulation of the quantity of protein produced. The disease should be of a recessive inheritance caused by the absence of a normally functioning copy of a gene. The target cells should be removed safely from the body for manipulation and then safely returned. The disease treatment should involve a target cell that is directly affected by the disease process. If an unaffected target cell is used, it must be able to produce a new gene product accessible to the abnormal cell. Section 4 Scientific Communications DECEMBER 2000 VOLUME 31, NUMBER 12 LABORATORY MEDICINE 6 7 5

5 (Target cells are hematopoietic stem cells or progenitor cells selected for insertion of normal genes.) The first gene therapy model employing cord blood was published in 1993 by researchers from the Herman B. Wells Center for Pediatric Research (Indianapolis, IN) using cord blood progenitor cells. 16 Using 2 retroviral vectors, the researchers found that the primitive cells in cord blood more efficiently transfected the adenosine deaminase (ADA) gene than did adult bone marrow cells. A deficiency of this enzyme is observed in severe combined immunodeficiency. Prenatal testing is available for ADA deficiency. This lends support to the use of cord blood primitive cells over primitive bone marrow cells, in that the latter are not as efficiently transduced with the normal ADA gene. Stem cells collected at birth can be utilized for gene transduction and then reinfused shortly after birth or frozen for future use. A year later, the same investigators found that ADA gene transduction into cord progenitor cells was significantly improved when fibronectin, an adhesion protein, was used in the culture, thus signifying that stem cell adhesion plays a role in the transduction process. In 1994, investigators at the University of Pittsburgh (Pittsburgh, PA) demonstrated successful transduction of a normal beta-glucocerebrosidase gene using the retroviral vector, MFG-GC. 17 CD34+ cells were isolated from cord blood and transduced in long-term bone marrow culture media with the MFG-GC retroviral vector. The beta-glucocerebrosidase enzyme activity was measured after the transduction period and the researchers determined that a shorter (2-day) transduction period yielded higher beta-glucocerebrosidase activity than the longer (5-day) transduction period, and that CD34+ cells from bone marrow exhibited lower enzyme activity than transduced CD34+ cells from cord blood. A deficiency of this enzyme leads to Gaucher disease, which is characterized as a rare familial disorder of fat metabolism, manifesting itself with hepatosplenomegaly, neurologic symptoms, and even death. Researchers at the University of Southern California School of Medicine in 1996 identified anti-hiv genes that, when introduced into immune cells, are capable of inhibiting the replication of the HIV-1 virus and thereby preserving their immune function. 18 Target cells for gene therapy include mature peripheral blood T lymphocytes and hematopoietic stem cells. The latter are preferred, owing to their ability to produce all cells involved in disease pathogenesis, including T lymphocytes. The researchers developed an in vitro model of this concept. Human CD34+ stem cells from umbilical cord blood were transduced with retroviral vectors carrying target protein for HIV-1. Stem cells were allowed to differentiate into myelomonocytic cells, where replication of the virus was measured. Inhibition of the HIV-1 virus was evident in cells containing the retrovector when compared with control cells. Further developments in 1998 by researchers at the Jikei University School of Medicine in Japan efficiently transferred the beta-glucuronidase gene using a retroviral vector to CD34+ stem cells from umbilical cord blood. 19 A deficiency in betaglucuronidase is the cause of mucopolysaccharidosis type VII (Sly syndrome). Persons with this disorder present with hepatosplenomegaly, joint abnormalities, corneal clouding, and Central Nervous System disorders due to the accumulation of glycosaminoglycans in the tissues. Premature death is common. Correction of this enzyme deficiency through gene therapy where a normal gene is transferred to the patient s DNA may relieve the patient of this debilitating disease. Other diseases in which treatment via gene therapy is likely to be helpful include argininosuccinic aciduria, citrullinemia, phenylketonuria, purine nucleoside phosphorylase deficiency, elliptocytosis, and granulocyte actin deficiency. 15 A timeline of cord blood research in the areas of transplantation, cord banking, and gene therapy is shown in the Figure. In addition to the material outlined above, numerous clinical trials involving umbilical cord blood commenced in the late 1990s as a result of the success of in vivo transplantation in earlier studies. A timeline of clinical trials involving umbilical cord blood is shown in Table

6 *SCID Gene Therapy model Thalassemia CB transplant *Dawn of CB banking (University of Arizona) *First Successful HLA-Mismatched CB Transplant (ALL) *EUROCORD *First SCA CB Transplant/ Blood Drive Cord blood timeline. ALL, acute lymphoblastic leukemia; CB, cord blood; SCID, Severe combined immunodeficiency. For member of EUROCORD and NETCORD, see the text. *First Successful HLA-Matched CB Transplant (Fanconi) *First CB Infused (Lymphangiosarcoma) NETCORD* *HIV-1 Gene Therapy Table 2. Timeline of Clinical Trials Involving Cord Blood 15 September 1997: Chemotherapy, radiation therapy, and umbilical cord blood transplantation for treating patients with hematologic cancer* September 1997: Blood bank established for gene therapy in HIV-infected infants January 1998: Umbilical cord blood transplantation for treating patients with severe aplastic anemia, malignant thymoma, or myelodysplasia * January 1998: Umbilical cord blood transplantation for treating patients with high-risk hematologic cancer* May 1998: Antiviral therapy plus either peripheral stem cell or umbilical cord blood transplantation for treating patients who are HIV positive and have hematologic cancer June 1998: Chemotherapy, radiation therapy, and umbilical cord blood transplantation for treating patients with hematologic cancer * August 1998: Umbilical cord blood transplantation for treating patients with hematologic cancer or other hematologic or metabolic disease* December 1998: Umbilical cord blood transplantation for treating patients with hematologic cancer or nonmalignant hematologic disease* *National Cancer Institute. National Institute of Allergy and Infectious Diseases. Conclusion In the latter half of the 20th century, investigators realized that a product of birth that is normally discarded is a rich source of viable stem cells capable of sustaining hematopoiesis in patients with hematologic disease. Another marvel of the 20 th century, the Internet, will play a dynamic role in database searches for persons in need of a compatible cord blood transplant. Due to the success of EUROCORD and NETCORD in European countries, it is almost commonplace for mothers preparing to deliver to at least be informed about cord blood collection and have the opportunity to donate cord blood for banking purposes. In the United States, the CBR prides itself in being the largest cord blood stem cell bank, with storage of more than 17,000 cord blood units. The continued success and progress of cord blood transplants, cord banking, and gene therapy has proven beneficial to patients with diseased bone marrow and will continue throughout the 21st century. l Acknowledgment I greatly acknowledge my mentor, Denise M. Harmening, PhD, for my cord blood research and for having faith in my abilities, and Norman Ende, MD, and Milton Ende, MD, for their lifesaving idea. Section 4 Scientific Communications DECEMBER 2000 VOLUME 31, NUMBER 12 LABORATORY MEDICINE 6 7 7

7 References 1. Ende M. Lymphangiosarcoma: report of a case. Pacific Med Sur. 1966;74: Ende M. History of umbilical cord blood transplantation. Lancet. 1995;346: Ende M, Ende N. Hematopoietic transplantation by means of fetal (cord) blood: a new method. V Med. 1972;99: Gluckman E, Broxmeyer HE, Auerbach AD, et al. Hematopoietic reconstitution in a patient with Fanconi s anemia by means of umbilical-cord blood from an HLA-identical sibling. N Engl J Med. 1989;321: Vilmer E, Sterkers G, Rahmy C, et al. HLA-mismatched cord blood transplantation in a patient with advanced leukemia. Transplantation. 1992;53: Shen BJ, Hou HS, Zhang HQ, et al. Unrelated, HLA-mismatched multiple human umbilical cord blood transfusion in four cases with advanced solid tumors: initial studies. Blood Cells. 1994;20: Issaragrisil S, Visuthisakchai S, Suvatte V, et al. Brief report: transplantation of cord-blood stem cells into a patient with severe thalassemia. N Engl J Med. 1994;332: Golden F. The sickle-cell kid. Time. 1999;154: Titus K. Cord blood banking: the birth of a new field. Lab Med. 1998;29: Rubinstein P, Adamson JW, Stevens C. The placental/umbilical cord blood program of the New York Blood Center: a progress report. Ann N Y Acad Sci. 1999;872: Rubenstein P, Carrier C, Scaradavou A, et al. Outcomes among 562 recipients of placental blood transplanted from unrelated donors, N Engl J Med. 1998;339: Weiner AW, Saculles F. Recruiting cord blood donors: spreading the word. AABB News. 2000;22: Gluckman E, Rocha V, Chastang C. European results of unrelated cord blood transplants. Bone Marrow Transplant. 1998;21(suppl 1):S87-S Hakenberg P, Kogler G, Wernet P. NETCORD: a cord blood allocation network. Bone Marrow Transplant. 1998;22(supple 1):S17-S Karson EM. Principles of gene transfer and the treatment of disease. Biotechnology. 1991;16: Moritz T, Keller DC, Williams DA. Human cord blood cells as targets for gene transfer: potential use in genetic therapies of severe combined immunodeficiency disease. J Exp Med. 1993;178: Bahnson AB, Nimgaonkar M, Fei Y, et al. Transduction of CD34+ enriched cord blood and Gaucher bone marrow cells by a retroviral vector carrying the glucocerebrosidase gene. Gene Ther. 1994;1: Bahner I, Kearns K, Hao QL, et al. Transduction of human CD34+ hematopoietic progenitor cells by a retroviral vector expressing an RRE decoy inhibits human immunodeficiency virus type 1 replication in myelomonocytic cells produced in long-term culture. J Virol. 1996;70: Ohashi T, Lizuka S, Sly WS, et al. Efficient and persistent expression of beta-glucuronidase gene in CD34+ cells from human umbilical cord blood by retroviral vector. Eur J Haematol. 1998;61:

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