Haematopoietic stem cell transplant patients have a high initial failure rate to hepatitis B vaccination that can be overcome with subsequent vaccination series Article Swipe
Reem Shalabi
,
Michelle Arielle Worst
,
Thomas E. Hughes
,
Tracey Walsh‐Chocolaad
,
Lisa Cook
,
Kristen Gunn
,
Brian Wells
,
Rodica Ciurea
,
Georg Aue
,
Xin Tian
,
Richard W. Childs
·
YOU?
·
· 2021
· Open Access
·
· DOI: https://doi.org/10.1111/bjh.17991
YOU?
·
· 2021
· Open Access
·
· DOI: https://doi.org/10.1111/bjh.17991
Recipient immunity is compromised following allogeneic haematopoietic stem cell transplantation (HSCT), necessitating prophylaxis with antimicrobial and antiviral agents and re-immunisation against viral and bacterial pathogens.1 Most patients lose protective hepatitis B virus (HBV) surface antibodies (anti-HBs) following conditioning therapy, hence post-HSCT HBV vaccination is imperative, particularly for those with a prior history of HBV infection at high risk for viral re-activation.2-4 The Infectious Diseases Society of America recommends initiating vaccination (including HBV) 6–12 months following HSCT to allow for reconstitution of cellular and humoral immunity.5 However, delayed immune reconstitution, exposure to immunosuppressive therapy (IST) and development of graft-versus-host disease (GVHD) can hinder the effectiveness of vaccines.6 The efficacy of HBV vaccination is not well-defined in transplant patients who continue to take IST and/or who have a history of or ongoing GVHD. Further, little data exist on the efficacy of HBV revaccination in patients who have failed to respond to the first vaccination series. This was a single-centre, retrospective analysis assessing the effectiveness of the HBV vaccine following HSCT and the impact of multiple factors on achieving successful seroconversion in patients undergoing one to four HBV vaccination series (Figure S1). We reviewed vaccine histories for a consecutive cohort of patients who received allogeneic HSCT on National Institutes of Health (NIH) Institutional Review Board (IRB)-approved protocols 99-H-0050, 08-H-0046 and 10-H-0154 between November 2006 and December 2015. Patients were included in the analysis if they received at least one three-dose series of recombinant HBV vaccine7 and had post-vaccine anti-HBs titers measured two months after the completion of each series, which represents the NIH institutional standard for recipients of allogeneic HSCT. The first HBV series were provided to chronic GVHD-free recipients at 12, 14, and 18 months post HSCT. Patients who had a negative or indeterminate anti-HBs titre following the first vaccine series were eligible to receive one or more additional HBV vaccine series. Additional three-dose series followed the 0-, 2-, and 6-months intervals although some intervals between doses were extended as patients who were further out from transplant had a decrease in the frequency of their follow-up visits. The study outcome was vaccine response, defined as the presence of a positive anti-HBs titre following the vaccination series (i.e., a titre of ≥10 mIU/ml, which is considered neutralising for HBV).8 Vaccine response rates over a series of vaccinations were estimated using Kaplan–Meier methods, censoring patients at the time of their last assessment. The association between response after the first vaccination series and baseline patient- and transplant-related factors (Table I) were assessed using logistic regression analysis. The study cohort included 52 HSCT patients (median age 22 years, range 17–62) with different diagnoses (Table I). The majority of patients underwent HSCT from human leucocyte antigen (HLA)-matched donors and received ciclosporin plus mini-dose methotrexate 5 mg/m2/dose at days +1, +3, +6 as GVHD prophylaxis, and the remaining patients received a combination of a single umbilical-cord-unit and CD34+ selected stem cells from a haploidentical relative, with mycophenolate and tacrolimus as GVHD prophylaxis. Twenty-seven (52%) patients received conditioning with anti-thymocyte globulin (ATG), fludarabine, and cyclophosphamide, eight (15%) were conditioned with fludarabine and cyclophosphamide, and 17 (33%) patients were conditioned with ATG, fludarabine, cyclophosphamide and low-dose (2 Gy) total body irradiation. A total of 39 (75%) patients were on IST [24 (46%) on prednisone] at the time of the first vaccination (Table SI). In this cohort, none of the patients received post-HSCT cyclophosphamide as GVHD prophylaxis. The median time to first HBV vaccination was 12 months (range 8–37) post-HSCT. Twenty-seven (52%) patients achieved immunity following the first vaccination series. Among those who failed to respond following the first or subsequent vaccination series, 19, four, and two patients received a second, third and fourth vaccine series respectively. The estimated cumulative anti-HBs response rates were 82%, 91% and 100% for the second to fourth vaccine series respectively (Fig 1A). A logistic regression analysis revealed patients who achieved a protective antibody response after the initial vaccination series had higher CD4 counts compared with those who failed to respond, with a median CD4 count of 450 vs 300/μl respectively (P = 0·024, Fig 1B). Patients with a history of acute GVHD were less likely to respond to the first vaccination series compared to those with no history of acute GVHD (vaccine response 37·9% vs 69·6%, P = 0·029). Other factors analysed, including pre-transplant HBV seropositivity, time from HSCT to initiation of vaccine, use of any IST agent or prednisone during vaccination, pre-vaccination lymphocyte count, CD8 count, and history and/or presence of chronic GVHD, were not found to be correlated with an anti-HBs response after the initial vaccination series. Five patients received rituximab within six months of HBV vaccination, two of which responded. Amongst the 15 patients that were vaccinated six or more months after receiving post-transplant rituximab, seven (47%) developed protective immunity with their first vaccination series. All patients at risk for HBV reactivation received lamivudine prophylaxis, therefore only two patients (3·8%) reactivated HBV and both subsequently responded to vaccination following one and four vaccination series. In this retrospective analysis, we observed an initial HBV vaccine response rate of only 52%, which was lower than the results reported by Jaffe and colleagues.9 Our analysis confirms their findings that a history of acute GVHD negatively impacted HBV vaccine response, and further identifies CD4 count to be a pre-vaccination predictor. However, the impact of chronic GVHD on HBV vaccine response could not be discerned from our analysis. Although a recent trial showed that response rates to HPV vaccinations are lower in transplant patients who remained on IST,10 vaccination of most patients in our study with chronic GVHD was delayed until their GVHD resolved and their immunosuppression could be tapered. Limitations of our study include: (i) this was a retrospective analysis and 73% of patients had aplastic anaemia, instead of a broader transplant population; and (ii) our lab provided qualitative anti-HBs titres (positive, negative or indeterminate) rather than quantitative titres. In conclusion, this study demonstrates a substantial proportion of HSCT patients receiving HBV vaccination will fail to respond to the first vaccination series, and that subsequent vaccination series can improve the rates of seroconversion. Lower pre-vaccination CD4 count and a history of acute GVHD were inversely associated with an initial vaccine response. Remarkably, we observed that with up to four repeat vaccination series, all evaluable patients developed a protective anti-HBs response. These results highlight the need to assess serologic response in HSCT patients following HBV vaccination and the utility of continuing vaccination until protective immunity is achieved, a recommendation not emphasised in current post-transplant vaccination guidelines. The authors would like to thank all the patients who participated in the clinical studies. This research was supported by the Intramural Research Program of the National Heart, Lung and Blood Institute (NHLBI), the Clinical Center, National Institutes of Health in Bethesda, Maryland, USA. MW, RAS, TWC, TH and RWC designed and wrote the protocol. GA, BW, LC and KG participated in patient care. MW and RAS contributed to data acquisition. RC and XT analysed the data. RAS, MW, XT, TWC and RWC wrote the paper. All authors reviewed and approved the final manuscript. The views expressed in this article are those of the author (TWC) and do not necessarily reflect the official policy or position of Fort Belvoir Community Hospital, the Defense Health Agency, Department of Defense, or US Government. TWC owns stock in Merck. RAS’s spouse is employed by GlaxoSmithKline. All other authors declare no competing financial interests. Table SI. Number of patients on immunosuppressive therapy (IST) and prednisone. Fig S1. Study flow diagram. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
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- Type
- letter
- Language
- en
- Landing Page
- https://doi.org/10.1111/bjh.17991
- https://onlinelibrary.wiley.com/doi/pdfdirect/10.1111/bjh.17991
- OA Status
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- Cited By
- 2
- References
- 10
- Related Works
- 10
- OpenAlex ID
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https://openalex.org/W4200128088Canonical identifier for this work in OpenAlex
- DOI
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https://doi.org/10.1111/bjh.17991Digital Object Identifier
- Title
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Haematopoietic stem cell transplant patients have a high initial failure rate to hepatitis B vaccination that can be overcome with subsequent vaccination seriesWork title
- Type
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letterOpenAlex work type
- Language
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enPrimary language
- Publication year
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2021Year of publication
- Publication date
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2021-12-08Full publication date if available
- Authors
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Reem Shalabi, Michelle Arielle Worst, Thomas E. Hughes, Tracey Walsh‐Chocolaad, Lisa Cook, Kristen Gunn, Brian Wells, Rodica Ciurea, Georg Aue, Xin Tian, Richard W. ChildsList of authors in order
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https://onlinelibrary.wiley.com/doi/pdfdirect/10.1111/bjh.17991Direct link to full text PDF
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bronzeOpen access status per OpenAlex
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https://onlinelibrary.wiley.com/doi/pdfdirect/10.1111/bjh.17991Direct OA link when available
- Concepts
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Medicine, Vaccination, Immunology, Seroconversion, Hepatitis B virus, Hepatitis B, Hematopoietic stem cell transplantation, Immunity, Transplantation, Internal medicine, Immune system, VirusTop concepts (fields/topics) attached by OpenAlex
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| abstract_inverted_index.had | 243, 287, 335, 654, 958 |
| abstract_inverted_index.lab | 970 |
| abstract_inverted_index.not | 112, 750, 895, 1082, 1197, 1260 |
| abstract_inverted_index.one | 181, 235, 303, 827 |
| abstract_inverted_index.our | 899, 926, 945, 969 |
| abstract_inverted_index.out | 332 |
| abstract_inverted_index.six | 769, 785 |
| abstract_inverted_index.the | 102, 136, 149, 160, 163, 169, 228, 251, 258, 295, 314, 339, 353, 361, 392, 403, 468, 545, 548, 558, 585, 596, 628, 650, 693, 760, 779, 851, 885, 1002, 1013, 1057, 1070, 1096, 1101, 1109, 1114, 1122, 1142, 1164, 1173, 1180, 1192, 1200, 1210, 1263, 1273, 1285, 1289 |
| abstract_inverted_index.two | 248, 605, 774, 815 |
| abstract_inverted_index.use | 728 |
| abstract_inverted_index.was | 154, 348, 573, 848, 931, 950, 1106 |
| abstract_inverted_index.who | 117, 123, 143, 199, 286, 329, 591, 643, 661, 917, 1098 |
| abstract_inverted_index.(Fig | 635 |
| abstract_inverted_index.(ii) | 968 |
| abstract_inverted_index.100% | 626 |
| abstract_inverted_index.1A). | 636 |
| abstract_inverted_index.1B). | 679 |
| abstract_inverted_index.2006 | 220 |
| abstract_inverted_index.52%, | 846 |
| abstract_inverted_index.82%, | 623 |
| abstract_inverted_index.ATG, | 521 |
| abstract_inverted_index.Five | 764 |
| abstract_inverted_index.Fort | 1206 |
| abstract_inverted_index.GVHD | 465, 492, 564, 686, 705, 868, 889, 930, 935, 1026 |
| abstract_inverted_index.HBV) | 71 |
| abstract_inverted_index.HSCT | 75, 167, 202, 426, 444, 723, 992, 1064 |
| abstract_inverted_index.Lung | 1117 |
| abstract_inverted_index.Most | 25 |
| abstract_inverted_index.RAS, | 1134, 1166 |
| abstract_inverted_index.S1). | 188 |
| abstract_inverted_index.SI). | 552 |
| abstract_inverted_index.TWC, | 1135 |
| abstract_inverted_index.This | 153, 1104 |
| abstract_inverted_index.USA. | 1132 |
| abstract_inverted_index.body | 529 |
| abstract_inverted_index.both | 821 |
| abstract_inverted_index.cell | 8 |
| abstract_inverted_index.data | 133, 1158 |
| abstract_inverted_index.days | 460 |
| abstract_inverted_index.each | 254 |
| abstract_inverted_index.fail | 998 |
| abstract_inverted_index.flow | 1253 |
| abstract_inverted_index.four | 183, 829, 1042 |
| abstract_inverted_index.from | 333, 445, 483, 722, 898 |
| abstract_inverted_index.have | 124, 144 |
| abstract_inverted_index.high | 56 |
| abstract_inverted_index.last | 396 |
| abstract_inverted_index.less | 688 |
| abstract_inverted_index.like | 1092 |
| abstract_inverted_index.lose | 27 |
| abstract_inverted_index.more | 305, 787 |
| abstract_inverted_index.most | 923 |
| abstract_inverted_index.need | 1058 |
| abstract_inverted_index.none | 556 |
| abstract_inverted_index.only | 814, 845 |
| abstract_inverted_index.over | 379 |
| abstract_inverted_index.owns | 1221 |
| abstract_inverted_index.plus | 454 |
| abstract_inverted_index.post | 283 |
| abstract_inverted_index.rate | 843 |
| abstract_inverted_index.risk | 57, 806 |
| abstract_inverted_index.some | 321 |
| abstract_inverted_index.stem | 7, 481 |
| abstract_inverted_index.take | 120 |
| abstract_inverted_index.than | 850, 980, 1278 |
| abstract_inverted_index.that | 782, 863, 906, 1007, 1038 |
| abstract_inverted_index.they | 231 |
| abstract_inverted_index.this | 554, 833, 949, 985, 1187 |
| abstract_inverted_index.time | 393, 546, 568, 721 |
| abstract_inverted_index.were | 225, 271, 299, 325, 330, 384, 415, 508, 518, 537, 622, 687, 749, 783, 1027 |
| abstract_inverted_index.will | 997 |
| abstract_inverted_index.with | 13, 48, 434, 487, 499, 510, 520, 659, 665, 681, 700, 755, 798, 928, 1030, 1039 |
| abstract_inverted_index.(15%) | 507 |
| abstract_inverted_index.(33%) | 516 |
| abstract_inverted_index.(46%) | 541 |
| abstract_inverted_index.(47%) | 794 |
| abstract_inverted_index.(52%) | 495, 580 |
| abstract_inverted_index.(75%) | 535 |
| abstract_inverted_index.(HBV) | 32 |
| abstract_inverted_index.(IST) | 93, 1247 |
| abstract_inverted_index.(NIH) | 208 |
| abstract_inverted_index.(TWC) | 1194 |
| abstract_inverted_index.2015. | 223 |
| abstract_inverted_index.Among | 589 |
| abstract_inverted_index.Blood | 1119 |
| abstract_inverted_index.Board | 211 |
| abstract_inverted_index.CD34+ | 479 |
| abstract_inverted_index.GVHD, | 748 |
| abstract_inverted_index.GVHD. | 130 |
| abstract_inverted_index.HSCT. | 266, 284 |
| abstract_inverted_index.Jaffe | 855 |
| abstract_inverted_index.Lower | 1017 |
| abstract_inverted_index.Other | 714 |
| abstract_inverted_index.Study | 1252 |
| abstract_inverted_index.Table | 1239 |
| abstract_inverted_index.These | 1054 |
| abstract_inverted_index.acute | 685, 704, 867, 1025 |
| abstract_inverted_index.after | 250, 402, 649, 759, 789 |
| abstract_inverted_index.agent | 732 |
| abstract_inverted_index.allow | 77 |
| abstract_inverted_index.care. | 1152 |
| abstract_inverted_index.cells | 482 |
| abstract_inverted_index.could | 894, 940 |
| abstract_inverted_index.count | 669, 878, 1020 |
| abstract_inverted_index.data. | 1165 |
| abstract_inverted_index.doses | 324 |
| abstract_inverted_index.eight | 506 |
| abstract_inverted_index.exist | 134 |
| abstract_inverted_index.final | 1181 |
| abstract_inverted_index.first | 150, 268, 296, 404, 549, 570, 586, 597, 694, 800, 1003 |
| abstract_inverted_index.found | 751 |
| abstract_inverted_index.four, | 603 |
| abstract_inverted_index.hence | 39 |
| abstract_inverted_index.human | 446 |
| abstract_inverted_index.least | 234 |
| abstract_inverted_index.lower | 849, 913 |
| abstract_inverted_index.note: | 1256 |
| abstract_inverted_index.other | 1232 |
| abstract_inverted_index.prior | 50 |
| abstract_inverted_index.range | 432 |
| abstract_inverted_index.rates | 378, 621, 908, 1014 |
| abstract_inverted_index.seven | 793 |
| abstract_inverted_index.stock | 1222 |
| abstract_inverted_index.study | 346, 422, 927, 946, 986 |
| abstract_inverted_index.thank | 1094 |
| abstract_inverted_index.their | 342, 395, 799, 861, 934, 938 |
| abstract_inverted_index.third | 610 |
| abstract_inverted_index.those | 47, 590, 660, 699, 1190 |
| abstract_inverted_index.titre | 293, 359, 366 |
| abstract_inverted_index.total | 528, 532 |
| abstract_inverted_index.trial | 904 |
| abstract_inverted_index.until | 933, 1075 |
| abstract_inverted_index.using | 386, 417 |
| abstract_inverted_index.views | 1184 |
| abstract_inverted_index.viral | 21, 59 |
| abstract_inverted_index.virus | 31 |
| abstract_inverted_index.which | 256, 370, 776, 847 |
| abstract_inverted_index.would | 1091 |
| abstract_inverted_index.wrote | 1141, 1172 |
| abstract_inverted_index.≥10 | 368 |
| abstract_inverted_index.(ATG), | 502 |
| abstract_inverted_index.(GVHD) | 99 |
| abstract_inverted_index.(Table | 413, 437, 551 |
| abstract_inverted_index.(i.e., | 364 |
| abstract_inverted_index.(other | 1277 |
| abstract_inverted_index.(range | 576 |
| abstract_inverted_index.37·9% | 708 |
| abstract_inverted_index.6–12 | 72 |
| abstract_inverted_index.HBV).8 | 375 |
| abstract_inverted_index.Health | 207, 1128, 1212 |
| abstract_inverted_index.Heart, | 1116 |
| abstract_inverted_index.IST,10 | 920 |
| abstract_inverted_index.Merck. | 1224 |
| abstract_inverted_index.Number | 1241 |
| abstract_inverted_index.Please | 1255 |
| abstract_inverted_index.Review | 210 |
| abstract_inverted_index.agents | 17 |
| abstract_inverted_index.and/or | 122, 744 |
| abstract_inverted_index.assess | 1060 |
| abstract_inverted_index.author | 1193, 1287 |
| abstract_inverted_index.cohort | 196, 423 |
| abstract_inverted_index.count, | 739, 741 |
| abstract_inverted_index.counts | 657 |
| abstract_inverted_index.donors | 450 |
| abstract_inverted_index.during | 735 |
| abstract_inverted_index.failed | 145, 592, 662 |
| abstract_inverted_index.fourth | 612, 631 |
| abstract_inverted_index.higher | 655 |
| abstract_inverted_index.hinder | 101 |
| abstract_inverted_index.immune | 87 |
| abstract_inverted_index.impact | 170, 886 |
| abstract_inverted_index.likely | 689 |
| abstract_inverted_index.little | 132 |
| abstract_inverted_index.median | 567, 667 |
| abstract_inverted_index.months | 73, 249, 282, 575, 770, 788 |
| abstract_inverted_index.paper. | 1174 |
| abstract_inverted_index.policy | 1202 |
| abstract_inverted_index.rather | 979 |
| abstract_inverted_index.recent | 903 |
| abstract_inverted_index.repeat | 1043 |
| abstract_inverted_index.second | 629 |
| abstract_inverted_index.series | 186, 237, 270, 298, 312, 363, 381, 406, 614, 633, 653, 696, 1010 |
| abstract_inverted_index.should | 1281 |
| abstract_inverted_index.showed | 905 |
| abstract_inverted_index.single | 476 |
| abstract_inverted_index.spouse | 1226 |
| abstract_inverted_index.titers | 246 |
| abstract_inverted_index.titres | 974 |
| abstract_inverted_index.within | 768 |
| abstract_inverted_index.years, | 431 |
| abstract_inverted_index.(3·8%) | 817 |
| abstract_inverted_index.(Figure | 187 |
| abstract_inverted_index.(HSCT), | 10 |
| abstract_inverted_index.(median | 428 |
| abstract_inverted_index.0·024, | 677 |
| abstract_inverted_index.300/μl | 673 |
| abstract_inverted_index.69·6%, | 710 |
| abstract_inverted_index.8–37) | 577 |
| abstract_inverted_index.Agency, | 1213 |
| abstract_inverted_index.America | 66 |
| abstract_inverted_index.Amongst | 778 |
| abstract_inverted_index.Belvoir | 1207 |
| abstract_inverted_index.Center, | 1124 |
| abstract_inverted_index.Defense | 1211 |
| abstract_inverted_index.Program | 1112 |
| abstract_inverted_index.RAS’s | 1225 |
| abstract_inverted_index.Society | 64 |
| abstract_inverted_index.Vaccine | 376 |
| abstract_inverted_index.against | 20 |
| abstract_inverted_index.antigen | 448 |
| abstract_inverted_index.article | 1188 |
| abstract_inverted_index.authors | 1090, 1176, 1233 |
| abstract_inverted_index.between | 218, 323, 400 |
| abstract_inverted_index.broader | 964 |
| abstract_inverted_index.chronic | 274, 747, 888, 929 |
| abstract_inverted_index.cohort, | 555 |
| abstract_inverted_index.content | 1264 |
| abstract_inverted_index.current | 1085 |
| abstract_inverted_index.declare | 1234 |
| abstract_inverted_index.defined | 351 |
| abstract_inverted_index.delayed | 86, 932 |
| abstract_inverted_index.disease | 98 |
| abstract_inverted_index.factors | 173, 412, 715 |
| abstract_inverted_index.further | 331, 875 |
| abstract_inverted_index.history | 51, 126, 683, 702, 743, 865, 1023 |
| abstract_inverted_index.humoral | 83 |
| abstract_inverted_index.improve | 1012 |
| abstract_inverted_index.initial | 651, 761, 839, 1032 |
| abstract_inverted_index.instead | 961 |
| abstract_inverted_index.mIU/ml, | 369 |
| abstract_inverted_index.missing | 1279 |
| abstract_inverted_index.ongoing | 129 |
| abstract_inverted_index.outcome | 347 |
| abstract_inverted_index.patient | 1151 |
| abstract_inverted_index.queries | 1276 |
| abstract_inverted_index.receive | 302 |
| abstract_inverted_index.reflect | 1199 |
| abstract_inverted_index.respond | 147, 594, 691, 1000 |
| abstract_inverted_index.results | 852, 1055 |
| abstract_inverted_index.second, | 609 |
| abstract_inverted_index.series, | 255, 601, 1005, 1045 |
| abstract_inverted_index.series. | 152, 309, 588, 763, 802, 831 |
| abstract_inverted_index.surface | 33 |
| abstract_inverted_index.therapy | 92, 1246 |
| abstract_inverted_index.titres. | 982 |
| abstract_inverted_index.utility | 1071 |
| abstract_inverted_index.vaccine | 165, 191, 297, 308, 349, 613, 632, 841, 872, 892, 1033 |
| abstract_inverted_index.visits. | 344 |
| abstract_inverted_index.(NHLBI), | 1121 |
| abstract_inverted_index.(vaccine | 706 |
| abstract_inverted_index.0·029). | 713 |
| abstract_inverted_index.17–62) | 433 |
| abstract_inverted_index.6-months | 318 |
| abstract_inverted_index.Although | 901 |
| abstract_inverted_index.Clinical | 1123 |
| abstract_inverted_index.December | 222 |
| abstract_inverted_index.Defense, | 1216 |
| abstract_inverted_index.Diseases | 63 |
| abstract_inverted_index.Further, | 131 |
| abstract_inverted_index.However, | 85, 884 |
| abstract_inverted_index.National | 204, 1115, 1125 |
| abstract_inverted_index.November | 219 |
| abstract_inverted_index.Patients | 224, 285, 680 |
| abstract_inverted_index.Research | 1111 |
| abstract_inverted_index.achieved | 582, 644 |
| abstract_inverted_index.although | 320 |
| abstract_inverted_index.anaemia, | 960 |
| abstract_inverted_index.analysed | 1163 |
| abstract_inverted_index.analysis | 158, 229, 640, 859, 953 |
| abstract_inverted_index.anti-HBs | 245, 292, 358, 619, 757, 973, 1052 |
| abstract_inverted_index.antibody | 647 |
| abstract_inverted_index.aplastic | 959 |
| abstract_inverted_index.approved | 1179 |
| abstract_inverted_index.article. | 1290 |
| abstract_inverted_index.assessed | 416 |
| abstract_inverted_index.authors. | 1274 |
| abstract_inverted_index.baseline | 408 |
| abstract_inverted_index.cellular | 81 |
| abstract_inverted_index.clinical | 1102 |
| abstract_inverted_index.compared | 658, 697 |
| abstract_inverted_index.confirms | 860 |
| abstract_inverted_index.content) | 1280 |
| abstract_inverted_index.continue | 118 |
| abstract_inverted_index.decrease | 337 |
| abstract_inverted_index.designed | 1139 |
| abstract_inverted_index.diagram. | 1254 |
| abstract_inverted_index.directed | 1283 |
| abstract_inverted_index.efficacy | 107, 137 |
| abstract_inverted_index.eligible | 300 |
| abstract_inverted_index.employed | 1228 |
| abstract_inverted_index.exposure | 89 |
| abstract_inverted_index.extended | 326 |
| abstract_inverted_index.findings | 862 |
| abstract_inverted_index.followed | 313 |
| abstract_inverted_index.globulin | 501 |
| abstract_inverted_index.immunity | 1, 583, 797, 1077 |
| abstract_inverted_index.impacted | 870 |
| abstract_inverted_index.include: | 947 |
| abstract_inverted_index.included | 226, 424 |
| abstract_inverted_index.logistic | 418, 638 |
| abstract_inverted_index.low-dose | 525 |
| abstract_inverted_index.majority | 440 |
| abstract_inverted_index.measured | 247 |
| abstract_inverted_index.methods, | 388 |
| abstract_inverted_index.multiple | 172 |
| abstract_inverted_index.negative | 289, 976 |
| abstract_inverted_index.observed | 837, 1037 |
| abstract_inverted_index.official | 1201 |
| abstract_inverted_index.patient- | 409 |
| abstract_inverted_index.patients | 26, 116, 142, 179, 198, 328, 390, 427, 442, 470, 496, 517, 536, 559, 581, 606, 642, 765, 781, 804, 816, 916, 924, 957, 993, 1048, 1065, 1097, 1243 |
| abstract_inverted_index.position | 1204 |
| abstract_inverted_index.positive | 357 |
| abstract_inverted_index.presence | 354, 745 |
| abstract_inverted_index.provided | 272, 971 |
| abstract_inverted_index.received | 200, 232, 452, 471, 497, 560, 607, 766, 810 |
| abstract_inverted_index.remained | 918 |
| abstract_inverted_index.reported | 853 |
| abstract_inverted_index.research | 1105 |
| abstract_inverted_index.resolved | 936 |
| abstract_inverted_index.respond, | 664 |
| abstract_inverted_index.response | 377, 401, 620, 648, 707, 758, 842, 893, 907, 1062 |
| abstract_inverted_index.revealed | 641 |
| abstract_inverted_index.reviewed | 190, 1177 |
| abstract_inverted_index.selected | 480 |
| abstract_inverted_index.standard | 261 |
| abstract_inverted_index.studies. | 1103 |
| abstract_inverted_index.supplied | 1271 |
| abstract_inverted_index.tapered. | 942 |
| abstract_inverted_index.therapy, | 38 |
| abstract_inverted_index.vaccine, | 727 |
| abstract_inverted_index.vaccine7 | 241 |
| abstract_inverted_index.08-H-0046 | 215 |
| abstract_inverted_index.10-H-0154 | 217 |
| abstract_inverted_index.Bethesda, | 1130 |
| abstract_inverted_index.Community | 1208 |
| abstract_inverted_index.GVHD-free | 275 |
| abstract_inverted_index.Hospital, | 1209 |
| abstract_inverted_index.Institute | 1120 |
| abstract_inverted_index.Maryland, | 1131 |
| abstract_inverted_index.Recipient | 0 |
| abstract_inverted_index.achieved, | 1079 |
| abstract_inverted_index.achieving | 175 |
| abstract_inverted_index.analysed, | 716 |
| abstract_inverted_index.analysis, | 835 |
| abstract_inverted_index.analysis. | 420, 900 |
| abstract_inverted_index.antiviral | 16 |
| abstract_inverted_index.assessing | 159 |
| abstract_inverted_index.bacterial | 23 |
| abstract_inverted_index.censoring | 389 |
| abstract_inverted_index.competing | 1236 |
| abstract_inverted_index.developed | 795, 1049 |
| abstract_inverted_index.diagnoses | 436 |
| abstract_inverted_index.different | 435 |
| abstract_inverted_index.discerned | 897 |
| abstract_inverted_index.estimated | 385, 617 |
| abstract_inverted_index.evaluable | 1047 |
| abstract_inverted_index.expressed | 1185 |
| abstract_inverted_index.financial | 1237 |
| abstract_inverted_index.follow-up | 343 |
| abstract_inverted_index.following | 4, 36, 74, 166, 294, 360, 584, 595, 826, 1066 |
| abstract_inverted_index.frequency | 340 |
| abstract_inverted_index.hepatitis | 29 |
| abstract_inverted_index.highlight | 1056 |
| abstract_inverted_index.histories | 192 |
| abstract_inverted_index.including | 717 |
| abstract_inverted_index.infection | 54 |
| abstract_inverted_index.intervals | 319, 322 |
| abstract_inverted_index.inversely | 1028 |
| abstract_inverted_index.leucocyte | 447 |
| abstract_inverted_index.mini-dose | 455 |
| abstract_inverted_index.post-HSCT | 40, 561 |
| abstract_inverted_index.protocol. | 1143 |
| abstract_inverted_index.protocols | 213 |
| abstract_inverted_index.publisher | 1258 |
| abstract_inverted_index.receiving | 790, 994 |
| abstract_inverted_index.relative, | 486 |
| abstract_inverted_index.remaining | 469 |
| abstract_inverted_index.responded | 823 |
| abstract_inverted_index.response, | 350, 873 |
| abstract_inverted_index.response. | 1034, 1053 |
| abstract_inverted_index.rituximab | 767 |
| abstract_inverted_index.serologic | 1061 |
| abstract_inverted_index.supported | 1107 |
| abstract_inverted_index.therefore | 813 |
| abstract_inverted_index.underwent | 443 |
| abstract_inverted_index.(anti-HBs) | 35 |
| abstract_inverted_index.(including | 70 |
| abstract_inverted_index.(positive, | 975 |
| abstract_inverted_index.99-H-0050, | 214 |
| abstract_inverted_index.Additional | 310 |
| abstract_inverted_index.Department | 1214 |
| abstract_inverted_index.Infectious | 62 |
| abstract_inverted_index.Institutes | 205, 1126 |
| abstract_inverted_index.Intramural | 1110 |
| abstract_inverted_index.additional | 306 |
| abstract_inverted_index.allogeneic | 5, 201, 265 |
| abstract_inverted_index.antibodies | 34 |
| abstract_inverted_index.associated | 1029 |
| abstract_inverted_index.completion | 252 |
| abstract_inverted_index.considered | 372 |
| abstract_inverted_index.continuing | 1073 |
| abstract_inverted_index.correlated | 754 |
| abstract_inverted_index.cumulative | 618 |
| abstract_inverted_index.emphasised | 1083 |
| abstract_inverted_index.identifies | 876 |
| abstract_inverted_index.immunity.5 | 84 |
| abstract_inverted_index.initiating | 68 |
| abstract_inverted_index.initiation | 725 |
| abstract_inverted_index.interests. | 1238 |
| abstract_inverted_index.lamivudine | 811 |
| abstract_inverted_index.lymphocyte | 738 |
| abstract_inverted_index.mg/m2/dose | 458 |
| abstract_inverted_index.negatively | 869 |
| abstract_inverted_index.post-HSCT. | 578 |
| abstract_inverted_index.predictor. | 883 |
| abstract_inverted_index.prednisone | 734 |
| abstract_inverted_index.proportion | 990 |
| abstract_inverted_index.protective | 28, 646, 796, 1051, 1076 |
| abstract_inverted_index.recipients | 263, 276 |
| abstract_inverted_index.recommends | 67 |
| abstract_inverted_index.regression | 419, 639 |
| abstract_inverted_index.represents | 257 |
| abstract_inverted_index.responded. | 777 |
| abstract_inverted_index.rituximab, | 792 |
| abstract_inverted_index.subsequent | 599, 1008 |
| abstract_inverted_index.successful | 176 |
| abstract_inverted_index.supporting | 1269 |
| abstract_inverted_index.tacrolimus | 490 |
| abstract_inverted_index.three-dose | 236, 311 |
| abstract_inverted_index.transplant | 115, 334, 915, 965 |
| abstract_inverted_index.undergoing | 180 |
| abstract_inverted_index.vaccinated | 784 |
| abstract_inverted_index.vaccines.6 | 105 |
| abstract_inverted_index.Government. | 1219 |
| abstract_inverted_index.Limitations | 943 |
| abstract_inverted_index.Remarkably, | 1035 |
| abstract_inverted_index.assessment. | 397 |
| abstract_inverted_index.association | 399 |
| abstract_inverted_index.ciclosporin | 453 |
| abstract_inverted_index.combination | 473 |
| abstract_inverted_index.compromised | 3 |
| abstract_inverted_index.conclusion, | 984 |
| abstract_inverted_index.conditioned | 509, 519 |
| abstract_inverted_index.consecutive | 195 |
| abstract_inverted_index.contributed | 1156 |
| abstract_inverted_index.development | 95 |
| abstract_inverted_index.fludarabine | 511 |
| abstract_inverted_index.guidelines. | 1088 |
| abstract_inverted_index.imperative, | 44 |
| abstract_inverted_index.information | 1270 |
| abstract_inverted_index.manuscript. | 1182 |
| abstract_inverted_index.necessarily | 1198 |
| abstract_inverted_index.pathogens.1 | 24 |
| abstract_inverted_index.population; | 966 |
| abstract_inverted_index.prednisone. | 1249 |
| abstract_inverted_index.prednisone] | 543 |
| abstract_inverted_index.prophylaxis | 12 |
| abstract_inverted_index.qualitative | 972 |
| abstract_inverted_index.reactivated | 818 |
| abstract_inverted_index.recombinant | 239 |
| abstract_inverted_index.responsible | 1261 |
| abstract_inverted_index.substantial | 989 |
| abstract_inverted_index.vaccination | 42, 69, 110, 151, 185, 362, 405, 550, 572, 587, 600, 652, 695, 762, 801, 825, 830, 921, 996, 1004, 1009, 1044, 1068, 1074, 1087 |
| abstract_inverted_index.Twenty-seven | 494, 579 |
| abstract_inverted_index.acquisition. | 1159 |
| abstract_inverted_index.colleagues.9 | 857 |
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| institutions_distinct_count | 11 |
| corresponding_institution_ids | https://openalex.org/I4210155647 |
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