CASE REPORT. Juno Yang, KMD, PhD 1,a Beom-Joon Lee, KMD, PhD 2,a and Jun-Hwan Lee, KMD, PhD 3,4#
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1 CASE REPORT CASE REPORTS OF IDIOPATHIC THROMBOCYTOPENIA UNRESPONSIVE TO FIRST-LINE THERAPIES TREATED WITH TRADITIONAL HERBAL MEDICINES BASED ON SYNDROME DIFFERENTIATION Juno Yang, KMD, PhD 1,a Beom-Joon Lee, KMD, PhD 2,a and Jun-Hwan Lee, KMD, PhD 3,4# The objective of our study is to present two cases showing the effects of traditional Korean herbal medicines based on traditional Korean medicine (TKM) for the treatment of immune thrombocytopenic purpura (ITP). One patient showed no response to treatment with steroids and an immunosuppressive agent. Moreover, liver toxicity and side effects of steroids were evident. However, after he ceased conventional treatment and started to take an herbal medicine, his liver function normalized and the steroid side effects resolved. Ultimately, he achieved complete remission. Another patient with ITP had sustained remission after steroid therapy in childhood, but extensive uterine bleeding and thrombocytopenia recurred when she was 16 years old. She was managed with steroids again for 2 years, but severe side effects occurred, and eventually she ceased taking steroids. She refused a splenectomy, and was then treated with a herbal medicine for 7 months, ultimately leading to sustained remission again. Many patients with resistance to first-line treatments tend to be reluctant to undergo a splenectomy, considered a standard second-line treatment. In conclusion, herbal medicines, based on TKM, may offer alternative treatments for persistent or chronic ITP that is resistant to existing first-line treatments. Keywords: idiopathic thrombocytopenic purpura, traditional Korean medicine, syndrome differentiation, herbal medicine (Explore 2016; ]:]]]-]]] & 2016 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license ( INTRODUCTION Primary idiopathic thrombocytopenic purpura (ITP) or primary immune thrombocytopenia, is characterized by platelet destruction (to o /L) in the absence of other causes or disorders that may be associated with thrombocytopenia. The main clinical challenge of primary ITP lies in the increased risk of bleeding, although bleeding symptoms, including epistaxis, petechiae, bruising, and purpura, are not always present. 1 1 Kyungheeyedang Oriental Medical Clinic, Suwon-City, Kyonggi-do, Republic of Korea 2 Division of Allergy, Immune and Respiratory System, Department of Internal Medicine, College of Korean Medicine, Kyung Hee University, Seoul, Republic of Korea 3 Clinical Research Division, Korea Institute of Oriental Medicine, Daejeon, Republic of Korea 4 Korean Medicine Life Science, University of Science & Technology (UST), Campus of Korea Institute of Oriental Medicine, Daejeon, Republic of Korea a Juno Yang and Beom-Joon Lee contributed equally as first author. # Correspondence to: 1672 Yuseong-daero, Yuseong-gu, Daejeon, 34054, Republic of Korea. omdjun@kiom.re.kr The primary first-line treatment of ITP is corticosteroids and intravenous immunoglobulin (IVIG) or anti-d globulin (anti- D). Corticosteroids are usually the first choice, and IVIG or anti-d is used as first-line treatment for patients for whom steroids are contraindicated. If first-line therapies fail, splenectomy, rituximab, immunosuppressive agents (e.g., cyclophosphamide and azathioprine), and thrombopoietin-receptor agonists (e.g., romiplostim and eltrombopag) may be considered as second-line treatments. 2,3 Splenectomy has also been regarded as a standard secondline treatment in the management of patients who are refractory to first-line treatments. Other second-line therapies are considered after the failure of splenectomy, but they are expensive and have various side effects. 3 However, many patients are reluctant to undergo a splenectomy because of the unpredictability of the response, 4 its invasiveness, 5 and possible complications. 6,7 Thus, many patients tend to postpone or avoid a splenectomy when possible. 8 Between adults and children with ITP, there are several clinical differences. In the case of adult ITP treatment, the spontaneous remission rate is lower, corticosteroids are used more frequently, and splenectomy is more often considered. 9 Syndrome differentiation is not only a typical traditional Korean medical diagnostic system but also a key concept in the practice of traditional Korean medicine (TKM). According & 2016 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license ( ISSN /$36.00 EXPLORE ] 2016, Vol. ], No. ] 1
2 to the syndrome differentiation diagnostic system, a disease can be categorized into any of several different patterns based on the analysis of clinical information obtained from the following four major traditional diagnostic procedures: observation, listening, questioning, and pulse analyses. These patterns are also used in traditional medical treatments, including the prescription of herbal medicine and acupuncture There have been some reports demonstrating the efficacy of herbal medicine instead of first-line treatments for ITP, 13,14 and there was one report of treatment of childhood persistent ITP with herbal medicine. 15 However, there has been no report demonstrating the effectiveness of herbal medicine in treating adult persistent or chronic ITP patients who were unresponsive to standard first-line therapies, based on the syndrome differentiation diagnostic system. Thus, in this article, we present two ITP patients, both of whom were unresponsive to the first-line treatment or discontinued conventional treatment due to the side effects of steroids. Nonetheless, they achieved complete or partial remission by taking herbal medicines based on syndrome differentiation without requiring a splenectomy. CASE 1 A 25-year-old male patient, a Korean student who resided in the Philippines, visited a local hospital with high fever (4401C) and a decreased platelet count (o /L) in January 2011, and was treated for dengue fever. The fever became stable after 1 week, but the thrombocytopenia persisted. A bone marrow biopsy showed moderate megakaryocytic hyperplasia, and treatment with oral prednisone 60 mg/d was started for newly diagnosed ITP on February 4. However, the patient was unresponsive to the treatment, and azathioprine 100 mg/d and prednisone 180 mg/d were administered orally on February 18. Subsequently, the patient started to suffer from side effects of the steroid, including weight gain and swelling, and liver toxicity was detected in a biochemical analysis on March 22. The azathioprine was replaced by cyclosporine 200 mg/d due to the liver toxicity. On April 26, because of persistent liver toxicity, the immunosuppressive drug cyclosporine was stopped, and prednisone was reduced to 60 mg/d. However, the platelet count still did not increase. Moreover, the patient could not walk properly due to vertebral pain, weight gain, and peripheral edema in both legs. The patient eventually came to Korea and visited our clinic in a wheelchair on August 5 (Fig. 1). On physical examination, the patient was unable to walk due to severe back pain and peripheral edema and had a cutaneous wound on his ankle that was not healing well. He was suffering from side effects of the steroid: moon face, edema, weight gain, muscle weakness, and pain in the back and knees. An erythematous facial complexion and dark redcolored tiny petechiae were observed around his trunk and neck. The patient also reported fatigue, mild irritability, insomnia, thirst, and yellow urine. A taut, rapid, and weak pulse was found on pulse examination. A dark red and dry tongue was observed. However, he had no bleeding symptoms, and no splenomegaly. Laboratory analyses showed a Fig. 1. Timeline of interventions and outcomes in case 1. PDN, prednisone; AZ, azathioprine; CS, cyclosporine; TKM, traditional Korean medicine, red arrow: TKM clinic visit day. platelet count of /L and aspartate aminotransferase (AST)/alanine transaminase (ALT) of 211/230 UI/L. The patient was taking oral prednisone 60 mg/d, calcium carbonate 40 mg/d, furocemide 40 mg/d, and celecoxib 400 mg/d. The patient was administered modified jigolpieum water extract orally (Table 1) three times per day under a diagnosis of persistent ITP, and furocemide was stopped. After three weeks, his platelet count increased to /L, and the AST/ALT ratio decreased to 130/150 UI/L. The prednisone was tapered down to 30 mg/d. However, the platelet count then fell to /L because of the reduced steroid dose. Thus, the herbal medicine was changed to a modified seongyutang with Salviae miltiorrhizae radix and Scutellariae radix water extract (Table 2). Subsequently, the platelet count increased again, and the AST/ALT ratio decreased gradually. After three months, the steroid was discontinued. After four months, the platelet counts and AST/ALT ratio were /L and 54/62 IU/L, respectively, the cutaneous wound had healed, and the general condition of the patient had improved. Thus, the dose of the herbal medicine was tapered to two-thirds the previous dose. After five months, the platelet counts and AST/ALT ratio were /L and 41/ 47 IU/L, respectively, indicating a complete response; however, the platelet count was maintained at /L 3. Given the patient's recovery, the herbal medicine was discontinued on January 7, Even with no medication, there was no bleeding sign, and the platelet count was still /L on May 15, 2014 (Fig. 2). CASE 2 This 20-year-old female patient suffered from a common cold when she was eight years old. A local pediatric doctor administered a cutaneous intermuscular injection of 2 EXPLORE ] 2016, Vol. ], No. ] ITP treated with traditional herbal medicines
3 Table 1. Ingredients and Doses of the Modified jigolpieum Water Extract Used in Case 1 and Activities of the Herbs Pharmaceutical Name Total Daily Dose (g/d) Main Activity of Herbal Drug in This Case Lycii radicis cortex 15 Clear deficiency in heat Moutan cortex 15 Activate blood and resolve stasis Ginseng radix 12 Tonify Qi and engender fluid Zingiberis rhizoma siccus 12 Tonify Qi and warm the interior Cinnamomi cortex spissus 12 Tonify Qi and tonify Yang Glycyrrhizae radix 6 Tonify Qi and harmonize Qi and blood Angelicae gigantis radix 6 Nourish Yin and harmonize the blood Cnidii rhizoma 6 Nourish Yin and activate blood; move Qi Paeoniae radix rubra 6 Nourish Yin and activated blood; resolve stasis Rehmanniae radix 6 Nourish Yin; enrich Yin; and subdue Yang Poria (Hoelen) 12 Drain dampness and invigorate spleen and stomach Alismatis rhizoma 12 Induce diuresis to alleviate edema antibiotics in her hip, which produced an extensive hematoma in the injected area. The patient was transferred to the emergency room and treated with IVIG; however, treatment with steroids was maintained under a diagnosis of ITP. A bone marrow biopsy revealed erythroid hyperplasia and increased megakaryocytes. Despite the severe side effects of the steroids (stomach irritation, swelling, weight gain, and moon face), the patient achieved a sustained remission approximately after six months. When the patient was 16 years old, she experienced extensive uterine bleeding, and her platelet count decreased to /L on January 10, She was treated with two cycles of IVIG, 1.0 g/kg/d intravenously for two days, and with oral steroids 60 mg/d based on a diagnosis of relapsed severe chronic ITP. She continued the oral steroid treatment for approximately two years, and she showed a partial response and sustained remission. However, the platelet count decreased to /L on February 2, Furthermore, steroids side effects such as bone pain, alopecia, weight gain, swelling, and fibromyalgia made the patient's symptoms much more serious. She finally stopped taking the steroids and visited our clinic seeking an alternative treatment on April 4, 2011 (Fig. 3). On physical examination, the patient had no bleeding or petechiae. Her general condition was poor, and she felt tired all the time. She was reported to have experienced lassitude, emaciation, low voice, dry mouth and throat, dizziness, mild insomnia, spontaneous sweating, intermittent palpitations, and delayed menstruation cycles. A thin, weak, and rapid pulse was noted on pulse examination. A pale tongue proper without coating was observed on tongue examination. She was treated with oral modified seongyutang with Salviae miltiorrhizae radix, Artemisiae apiaceae herba, Lycii radicis cortex, Biotae cacumen, andlonicerae flos water extract (Table 3) three times per day. Although her platelet count temporarily fell to /L due to hives, supposedly caused by the summer heat, her platelet count increased gradually for seven months. On November 11, 2011, her platelet count was maintained at /L and we stopped the herbal medicine and continued to observe the patient. Since then, there has been no bleeding sign; her platelet count was /L on July 6, 2012, and /L on June 5, 2014 (Fig. 4). Table 2. Ingredients and Doses of the Modified seongyutang Water Extract Used in Case 1 and Activities of the Herbs Pharmaceutical Name Total Daily Dose (g/d) Main Activity of Herbal Drug in this Case Astragali radix 30 Tonify Qi and secure the exterior Ginseng radix 12 Tonify Qi and engender fluid Zingiberis rhizoma siccus 12 Tonify Qi and warm the interior Cinnamomi cortex spissus 12 Tonify Qi and tonify Yang Glycyrrhizae radix 6 Tonify Qi; harmonize Qi and blood Angelicae gigantis radix 6 Nourish Yin and harmonize the blood Cnidii rhizoma 6 Nourish Yin, activate blood, and move Qi Paeoniae radix rubra 6 Nourish Yin and activated blood; resolve stasis Rehmanniae radix 6 Nourish Yin; enrich Yin; and subdue Yang Atractylodis rhizoma 6 Resolve dampness to move Qi and fortify the spleen Salviae miltiorrhizae radix 15 Tonify blood and activated blood to resolve stasis Scutellariae radix 15 Purge fire, clear heat, and detoxify ITP treated with traditional herbal medicines EXPLORE ] 2016, Vol. ], No. ] 3
4 Fig. 2. Changes in platelet counts and AST/ALT ratio during the course of treatment in case 1. Plt, platelets; AST, aspartate aminotransferase; ALT, alanine transaminase. DISCUSSION Primary ITP is an acquired autoimmune disorder characterized by a low platelet count in the peripheral blood without any recognized cause, mediated by platelet antibodies that accelerate platelet destruction, and inhibit their production. 2,16 Population-based studies have estimated the incidence of ITP to be per 100,000 children and 3.3 per 100,000 adults per year. 17 However, although two-thirds of newly diagnosed Fig. 3. Timeline of interventions and outcomes in case 2. PDN, prednisone; IVIG, intravenous immunoglobulin, red arrow: TKM clinic visit day. children obtain complete responses with the first-line treatment, 30% of children with newly diagnosed ITP progress to persistent or chronic ITP. 18 In Korea, % of children with ITP develop persistent or chronic ITP, 19 whereas 60% of adults with newly diagnosed ITP maintain a response after initial treatment with standard first-line therapies, although most adult patients exhibit chronic relapse after one year. 20,21 Second-line therapies, including splenectomy, rituximab, immunosuppressive agents (e.g., cyclophosphamide and azathioprine), and thrombopoietic-receptor agonists (e.g., romiplostim and eltrombopagand), are indicated for those patients who are unresponsive to or relapse after initial first-line therapies. 3 For decades, splenectomy has been considered a standard second-line therapy because it is highly effective and inexpensive compared with other second-line therapies. 2,22 Additionally, each of the other second-line therapies has unique potential toxicities, such as immune suppression, secondary malignancies, hypertension, and hepatic toxicity. Thus, splenectomy has been recommended for patients who fail corticosteroid therapy. 3 Nevertheless, the number of patients who opt to avoid a splenectomy has increased. 5,23 Many patients are simply reluctant to remove a healthy organ that has multiple hematological and immunological functions, and to undergo an invasive and irreversible procedure. Moreover, the procedure itself can cause mortality and increases the morbidity of various complications, including bacterial sepsis, 7 vascular disease such as venous thromboembolism or atherosclerosis, 24 thrombosis, 25 prolonged hospitalization, readmission to the hospital, and the requirement of additional interventions. 6,8 In children, in particular, postsplenectomy sepsis has risen to 3%, and an increased risk of sepsis probably persists for life. 2 In Korea, there are various norms for ITP treatment. Most patients receive their initial diagnosis and management from a 4 EXPLORE ] 2016, Vol. ], No. ] ITP treated with traditional herbal medicines
5 Table 3. Ingredients and Doses in the Modified seongyutang Water Extract Used in Case 2 and Activities of the Herbs Pharmaceutical Name Total Daily Dose (g/d) Main Activity of Herbal Drug in this Case Astragali radix 30 Tonify Qi and secure the exterior Ginseng radix 12 Tonify Qi and engender fluid Zingiberis rhizoma siccus 12 Tonify Qi and warm the interior Cinnamomi cortex spissus 12 Tonify Qi and tonify Yang Glycyrrhizae radix 6 Tonify Qi; harmonize Qi and blood Angelicae gigantis radix 6 Nourish Yin and harmonize the blood Cnidii rhizoma 6 Nourish Yin, activate blood, and move Qi Paeoniae radix rubra 6 Nourish Yin and activated blood; resolve stasis Rehmanniae radix 6 Nourish Yin; enrich Yin; and subdue Yang Salviae miltiorrhizae radix 15 Tonify blood and activated blood; resolve stasis Artemisiae apiaceae herba 6 Clear heat to cool the blood Lycii radicis cortex 15 Clear deficiency heat Biotae cacumen 30 Dissipate blood stasis and resolve phlegm Lonicerae flos 6 Clear heat to cool the blood and detoxify hematologist and routinely undergo a bone marrow examination. Regarding treatment, corticosteroids and anti-d are used commonly as first-line pharmacological treatments over IVIG, and splenectomy is generally considered for ITP patients who show first-line treatment resistance. 26,27 Nonetheless, because of complications, many patients in Korea have also been opting to defer a splenectomy as long as possible, and the need for alternative therapies before splenectomy to manage ITP unresponsive to first-line therapy has, therefore, increased. The main treatment goal in all ITP patients must be to maintain a safe platelet count, that is, not to normalize the platelet count, but keep it at a level that will prevent or stop major bleeding. However, no treatment objective in persistent or chronic ITP has been firmly defined as yet, and it is often driven by the desire to postpone or avoid the risks of more extreme treatments such as a splenectomy or immunosuppression. 28 Generally, most fatal bleeding has been reported to occur in ITP patients whose platelet counts were o /L. Thus, a platelet count of /L is generally considered safe for patients who do not perform physical labor, such as Fig. 4. Changes in platelet counts during the course of treatment in case 2. carpenters or farmers. 29 In this study, we defined remission as Z26 consecutive weeks of a platelet count Z /L after discontinuing the herbal medicine with no other ITP treatment, 30 and complete remission was defined as a platelet count Z /L. Traditional herbal medicine has been used for thousands of years in Korea. From the point of view of pathology, in traditional medicine based on syndrome differentiation, ITP is caused by blood heat expelling the blood from the vessels, which induces bleeding, such as epistaxis, plurimenorrhea, ulemorrhagia, and petechiae. After bleeding, the extravasated blood stagnates in the body (blood stasis) and inhibits circulation, so as to aggravate the bleeding. 31 In the chronic stage, the retained blood heat and extravasated blood, which act like toxins, can exhaust Qi and Yin, resulting in their deficiency. 32 Thus, chronic ITP is treated primarily by dissipating blood heat, removing toxins, promoting blood circulation, and by tonifying Qi and nourishing Yin. 33,34 In Case 1, the patient was treated with prednisone as an initial therapy. Prednisone generally shows an initial response within two weeks, 2 but the patient was unresponsive to the steroid. Thus, an immunosuppressant was added, and the steroid dose was increased. However, the patient failed to show any response over three months, and he experienced side effects, including liver toxicity. The patient ceased the ongoing conventional therapies and visited our clinic when the disease had progressed to a chronic stage. We diagnosed him with persistent ITP and a blood heat predominant pattern, based on Yin and Qi deficiency complex syndrome, according to the traditional syndrome differentiation diagnosis system. Thus, we administered a modified jigolpium water extract to initially clear the toxins including the blood heat. He responded well, and the steroid was tapered, but his platelet count then decreased again. Next, we changed the herbal medicine to a modified seongyutang water extract, invigorating the Qi and Yin to promote blood circulation. After that, he showed a continued complete response, and we discontinued the herbal treatment. Three years later, he exhibited sustained complete ITP treated with traditional herbal medicines EXPLORE ] 2016, Vol. ], No. ] 5
6 remission, defined, as above, by a platelet count /L without treatment. In Case 2, the patient experienced sustained remission after steroid therapy in childhood, but thrombocytopenia recurred with a low platelet level, /L, in January She started to undergo ITP treatment again and continued to take oral steroids with a platelet count /L for two years. However, after two years of treatment, she had to discontinue the steroid treatment because of side effects. She visited our clinic for an alternative therapy, and we diagnosed her with a blood-heat subordinate pattern based on Qi and Yin deficiency complex syndrome. Thus, we treated her with a modified seongyutang water extract for seven months. She showed a continued partial response, defined as platelet count /L. 3 Given her busy schedule, the absence of bleeding allowed us to discontinue the herbal medicine and to apply a watchful observation strategy. 29 At about two years later, her remission continued. In conclusion, herbal medicine based on TKM offers potential alternative therapies for patients with persistent or chronic ITP who do not respond sufficiently to the first-line treatments: corticosteroids, IVIG, and anti-d. Still, very little is known about the biological mechanism of traditional herbal medicines, and only limited data were generated in this study. Thus, further studies, including case control studies and randomized control trials with larger population sizes, are needed to demonstrate the efficacy, safety, and biological mechanism of herbal medicines in the treatment of ITP. CONFLICTS OF INTEREST The authors declare that they have no conflict of interest regarding the publication of this article. The English in this document has been checked by at least two professional editors, both native speakers of English. For a certificate, please see pklssi Acknowledgments This research was supported by the Korea Institute of Oriental Medicine, South Korea (K16121) REFERENCES 1. Cines DB, Blanchette VS. Immune thrombocytopenic purpura. N Engl J Med. 2002;346(13): Provan D, Stasi R, Newland AC, et al. International consensus report on the investigation and management of primary immune thrombocytopenia. Blood. 2010;115(2): Neunert C, Lim W, Crowther M, Cohen A, Solberg L, Crowther MA. The American Society of Hematology 2011 evidence-based practice guideline for immune thrombocytopenia. Blood. 2011;117(16): Balagué C, Vela S, Targarona E, et al. Predictive factors for successful laparoscopic splenectomy in immune thrombocytopenic purpura. Surg Endosc. 2006;20(8): Janssens A, Lambert C, Bries G, Bosly A, Selleslag D, Beguin Y. Primary immune thrombocytopenia in adults. Belg J Hematol. 2013;4(1): Kojouri K, Vesely SK, Terrell DR, George JN. 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