Toxicities of radiation treatment for breast cancer risks and management strategies jean l. wright -
Toxicities of Radiation Treatment for Breast Cancer Risks and Management Strategies Jean L. Wright
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Prevention and Management of Acute and Late Toxicities in Radiation Oncology Ugur Selek
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I would like to dedicate this book to all of our patients who have bravely managed the side effects of radiation therapy for breast cancer and to all the clinicians who work to minimize and manage these toxicities for our patients.
Preface
As a physician, I have always been interested in how to balance the risk of toxicity related to our treatment recommendations versus the potential benefits. In breast cancer, in particular, I found that this risk-benefit assessment plays into almost every treatment decision and that “gray zone” cases, where there is no clear-cut management pathway, make up the majority of the cases I see. The decision tree has innumerable branches: whether to treat at all, what to treat (whole breast? partial breast? low axilla? supraclavicular nodes? internal mammary nodes? and so on), and how to treat (compromise coverage of internal mammary nodes to reduce cardiac dose? prescribe to a higher isodose line to avoid a hotspot? utilize tissue equivalent bolus in a reconstructed chest wall?). Each branch of this decision tree requires a balanced assessment of risk versus benefit.
In light of the daily challenges we all face in optimizing this balance for our patients, I submitted a session to ASTRO’s annual meeting in 2017 called “Late Toxicity of Radiation for Breast Cancer: Overblown or Under-Appreciated?” and had the opportunity to chair the session. In that session, we focused on four management issues from the perspective of late toxicity: cardiac toxicity, lymphedema, impact of radiation on reconstruction, and second malignancy risk. And in preparing for that session, I became all the more aware of the magnitude of this topic and the many toxicities, both acute and late, which we did not have time to address in that session.
After the session was accepted, I was approached by the staff of Springer to inquire whether this topic might be suitable for a textbook, a question to which I readily answered “Yes!”
This book, then, has its origins in that 2017 ASTRO educational session and is an expansion of the four topics we addressed then into a longer list of both acute and late toxicities associated with radiation therapy for breast cancer. The book represents an attempt to compile a comprehensive list of all of the different types of toxicities that we encounter in managing our breast cancer patients. I sought out authors with published experience in their topic and was extremely fortunate to be able to assemble a team with expertise, experience, writing skills, and willingness
to contribute. I am very grateful to all of the authors of this work for their time and hard work in putting together this book. Together, we hope that this work proves a valuable resource to clinicians in radiation oncology clinics who care for our patients.
The book is primarily directed toward radiation oncology physicians, physician extenders (who are more and more often providing long-term follow-up for our patients), and nurses. I hope it may also be of use to other providers who see our patients during and after radiation treatment including medical oncologists and primary care physicians, as well as other members of our clinical teams who help to manage our patients.
In addition to the authors of this work, I would like to thank the staff of Springer, who provided so much support during this process, including Margaret Moore and Rekha Udaiyar.
Baltimore, MD, USA
Including Toxicity Risk in Balanced Clinical Decision Making
Jean L. Wright
Acute and Late Skin Toxicity from Breast Radiation
Lindsey Sloan and Sara Alcorn
Fatigue Associated with Radiation Treatment for Breast Cancer
Canhua Xiao and Mylin Ann Torres
Pain Associated with Radiation Treatment for Breast Cancer
Eunkyung Lee, Shannon Snyder, and Jennifer J. Hu
Considerations for Post-Mastectomy Radiation Therapy in the Setting of Breast Reconstruction
Lisa Singer and Jean L. Wright
Lymphedema After Breast Cancer Treatment
Kayla M. Daniell, Tessa C. Gillespie, Cheryl L. Brunelle, and Alphonse G. Taghian
Cardiotoxicity Associated with Radiation for Breast Cancer
Kara Lynne Leonard and David E. Wazer
Second Malignancies after Radiation for Breast Cancer
Sarah Nicole Hamilton
Tissue Fibrosis after Radiation Treatment for Breast Cancer
Kristin A. Plichta, Wenqing Sun, and John M. Buatti
Pulmonary Toxicity Associated with Radiation Treatment for Breast Cancer
Arti Parekh
Integrative Methods for Management of Toxicities Associated with Radiation Treatment for Breast Cancer
Meghana Reddy, Gautam Krishna Koipallil, and Amber Orman
Index
Contributors
Sara Alcorn, MD, MPH Department of Radiation Oncology and Molecular Radiation Sciences, Johns Hopkins University, Baltimore, MD, USA
Cheryl L. Brunelle, PT, CSS, CLT Department of Physical and Occupational Therapy, Massachusetts General Hospital, Boston, MA, USA
John M. Buatti, MD Department of Radiation Oncology, University of Iowa Hospitals and Clinics, Iowa City, IA, USA
Kayla M. Daniell, BS Department of Radiation Oncology, Massachusetts General Hospital, Boston, MA, USA
Tessa C. Gillespie, BS Department of Radiation Oncology, Massachusetts General Hospital, Boston, MA, USA
Sarah Nicole Hamilton, MD, FRCPC BC Cancer – Vancouver Centre, Vancouver, British Columbia, Canada
University of British Columbia, Vancouver, British Columbia, Canada
Jennifer J. Hu, PhD Department of Public Health Sciences, University of Miami School of Medicine, Miami, FL, USA
Gautam Krishna Koipallil, BS USF Morsani College of Medicine, MS2, Tampa, FL, USA
Eunkyung Lee, PhD, MS, RDN Department of Health Sciences, College of Health Professions and Sciences, Academic Health Sciences Center, University of Central Florida, Orlando, FL, USA
Kara Lynne Leonard, MD Department of Radiation Oncology, Lifespan Cancer Institute, Rhode Island Hospital, Warren Alpert Medical School of Brown University, Providence, RI, USA
Department of Radiation Oncology, Tufts Medical Center, Tufts University School of Medicine, Boston, MA, USA
Amber Orman, MD Department of Radiation Oncology, AdventHealth Medical Group, Orlando, FL, USA
University of Central Florida College of Medicine, Orlando, FL, USA
Arti Parekh, MD Allegheny General Hospital, Pittsburgh, PA, USA
Kristin A. Plichta, MD, PhD Department of Radiation Oncology, University of Iowa Hospitals and Clinics, Iowa City, IA, USA
Meghana Reddy, BS University of South Florida, Tampa, FL, USA
Lisa Singer, MD, PhD Department of Radiation Oncology, Dana-Farber Cancer Institute and Brigham and Women’s Hospital, Boston, MA, USA
Lindsey Sloan, MD, PhD Department of Radiation Oncology and Molecular Radiation Sciences, Johns Hopkins University, Baltimore, MD, USA
Shannon Snyder, BS Department of Health Sciences, College of Health Professions and Sciences, Academic Health Sciences Center, University of Central Florida, Orlando, FL, USA
Wenqing Sun, MD, PhD Department of Radiation Oncology, University of Iowa Hospitals and Clinics, Iowa City, IA, USA
Alphonse G. Taghian, MD, PhD Department of Radiation Oncology, Massachusetts General Hospital, Boston, MA, USA
Mylin Ann Torres, MD Department of Radiation Oncology, Winship Cancer Institute, Emory University School of Medicine, Atlanta, GA, USA
David E. Wazer, MD Department of Radiation Oncology, Lifespan Cancer Institute, Rhode Island Hospital, Warren Alpert Medical School of Brown University, Providence, RI, USA
Department of Radiation Oncology, Tufts Medical Center, Tufts University School of Medicine, Boston, MA, USA
Jean L. Wright, MD Johns Hopkins University, Department of Radiation Oncology and Molecular Radiation Sciences, Baltimore, MD, USA
Canhua Xiao, MD Department of Radiation Oncology, Winship Cancer Institute, Emory University School of Medicine, Atlanta, GA, USA
Including Toxicity Risk in Balanced Clinical Decision Making
Jean L. Wright
Adjuvant radiotherapy has been an established component of curative therapy for early-stage and locally advanced breast cancer for decades. Millions of women have received this form of therapy, and millions more will go on to receive radiation for breast cancer in the future. From the earliest studies that led to the shift from mastectomy to breast conservation for a majority of women with breast cancer [1, 2], the role of radiation has been to allow for less disfiguring and morbid breast cancer management. The introduction of radiotherapy into breast cancer management was fundamentally driven by the goal to allow for breast conservation and was an early element of the movement toward less toxic and more patient-centric care in breast cancer.
Since the initial studies establishing the role of adjuvant radiation for breast cancer, there have been significant improvements in all realms of breast cancer management, from diagnostic imaging, surgical techniques, and tailored systemic therapies to radiotherapy. These improvements have translated into improved outcomes for breast cancer patients, with 85% of patients with nonmetastatic disease expecting long-term survival from the disease [3]. Longer survival has in turn shifted the focus in breast cancer therapy toward preventing, minimizing, and managing the toxicities of treatment.
Clinical decision-making has always relied on a balanced assessment of the benefit of therapy, generally a reduction in the risk of cancer recurrence and in some cases an expected improvement in long-term survival versus the risks and side effects of treatment. This balance has become all the more challenging in the modern era of excellent outcomes for breast cancer patients.
Let’s take the example of the recent publication of the National Cancer Institute of Canada’s MA.20 study, which compared outcomes in women with early-stage
J. L. Wright (*)
Johns Hopkins University, Department of Radiation Oncology and Molecular Radiation Sciences, Baltimore, MD, USA
J. L. Wright (ed.), Toxicities of Radiation Treatment for Breast Cancer, https://doi.org/10.1007/978-3-030-11620-0_1
breast cancer with and without regional lymph node irradiation in addition to standard whole-breast radiation [4]. This study demonstrated improvements in both locoregional control and distant disease-free survival with the addition of regional lymph node radiation; at 10-year follow-up, distant disease-free survival was 75% in the breast-only arm vs 78% in the breast plus nodal radiation arm, a 3% improvement with no overall survival advantage seen. The likelihood of benefit was also seen to vary within subsets of patients, with those with estrogen receptor-negative disease seeing a greater improvement in outcome.
At the same time, as we will see in the detailed analyses in this book, the addition of regional nodal irradiation may also confer an increased risk of cardiac morbidity, radiation pneumonitis, lymphedema, and other toxicities, depending on the unique details of the patient’s case. In many cases the benefits and side effects of treatment may be quite modest, and there is often not a clearly superior treatment recommendation. The most recent guideline regarding the utilization of postmastectomy radiation summarizes this quandary in its overall statement: “The panel unanimously agreed that available evidence shows that post-mastectomy radiation reduces the risks of locoregional failure, any recurrence, and breast cancer mortality for patients with T1–2 breast cancer with one to three positive axillary nodes. However, some subsets of these patients are likely to have such a low risk of locoregional failure that the absolute benefit of post-mastectomy radiation is outweighed by its potential toxicities. In addition, the acceptable ratio of benefit to toxicity varies among patients and physicians. Thus, the decision to recommend post-mastectomy radiation requires a great deal of clinical judgment.” [5] Thus, the process of weighing the relatively small expected benefit of regional nodal irradiation vs the toxicities that may accompany it has become increasingly complex in the modern era.
In light of this increased recognition of the importance of toxicity from breast cancer therapy in clinical decision-making, this textbook serves as a review of the common toxicities associated with radiation for breast cancer. Each of the first nine chapters focuses on a specific toxicity type and reviews the existing literature regarding both acute and long-term manifestations of the toxicity. Embedded in each chapter are considerations for managing these toxicities, including reducing the risk and severity of toxicity, as well managing side effects when they occur. The tenth and final chapter addresses integrative therapy approaches as an overall approach to patient wellness during and after therapy.
While the approaches to managing toxicity vary with each type, a single overall theme emerges: the imperative to consider decisions and techniques that will minimize radiation exposure when not expected to compromise oncologic outcomes. The clearest means of avoiding a toxicity is to avoid the exposure, and thus the first clinical decision is whether radiation is indicated at all.
This critical decision of whether or not to recommend radiation is exemplified in the ongoing work to identify low-risk cohorts in women with breast cancer, in whom de-escalation of therapy may be appropriate. Women 70 and older with hormone receptor-positive early-stage breast cancer have been identified as a particularly low-risk group based on the results of the randomized CALGB study 9343, first published in 2004 with 10-year follow-up in 2013 [6]. This study demonstrated
J. L. Wright
a modest improvement in locoregional recurrence, from 10% to 2% with the addition of radiation to endocrine therapy after breast-conserving surgery, but there was no difference in overall survival or metastasis-free survival. This publication led to an update in the National Comprehensive Cancer Network (NCCN) treatment guidelines in 2004 to include a category 1 recommendation that after breastconserving surgery “breast irradiation may be omitted in those 70 years of age or older with estrogen-receptor positive, clinically node-negative, T1 tumors who receive adjuvant endocrine therapy.” Studies are now ongoing to identify younger patients who are at similarly low risk of locoregional recurrence, utilizing genomic risk scores in addition to other clinical factors. However, factors that contribute to decisions regarding radiation utilization in low-risk populations are not well understood; there is a growing body of work that seeks to understand the decision-making process between patients and physicians and to elucidate the factors that contribute to the ultimate treatment choice the patient makes and subsequent quality of life. Toxicity considerations are paramount in this decision process.
If the decision to treat is made, then effort must be directed at appropriately minimizing the intensity of therapy, including judicious utilization of nodal irradiation, hypofractionated treatment regimens, and partial breast irradiation. In addition, modern technology may be used to minimize normal tissue exposure. Breath hold is arguably the most important widely available technique for cardioprotection, and the ongoing RADCOMP study comparing photon vs proton radiation for patients receiving internal mammary node radiation will determine if reduction in cardiac exposure translates to decreased cardiac morbidity.
Despite efforts toward tailored treatment decisions and minimization of radiation exposure, toxicities of treatment remain a reality and an expected outcome from breast radiation. Thus, each chapter also discusses proactive management strategies that may be considered on a patient-specific level. It is our hope that this book will help radiation oncology clinicians of all kinds to better understand toxicity risks, will encourage consideration of toxicity in balanced clinical decision-making for our patients, and will offer some practical approaches to managing toxicities both preventively and as they arise.
References
1. Early Breast Cancer Trialists’ Collaborative G, Darby S, McGale P, Correa C, Taylor C, Arriagada R, et al. Effect of radiotherapy after breast-conserving surgery on 10-year recurrence and 15-year breast cancer death: meta-analysis of individual patient data for 10,801 women in 17 randomised trials. Lancet. 2011;378(9804):1707–16.
2. Fisher B, Anderson S, Bryant J, Margolese RG, Deutsch M, Fisher ER, et al. Twenty-year follow-up of a randomized trial comparing total mastectomy, lumpectomy, and lumpectomy plus irradiation for the treatment of invasive breast cancer. N Engl J Med. 2002;347(16):1233–41.
3. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2017. CA Cancer J Clin. 2017;67(1):7–30.
4. Whelan TJ, Olivotto IA, Levine MN. Regional nodal irradiation in early-stage breast cancer. N Engl J Med. 2015;373(19):1878–9.
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5. Recht A, Comen EA, Fine RE, Fleming GF, Hardenbergh PH, Ho AY, et al. Postmastectomy radiotherapy: an American Society of Clinical Oncology, American Society for Radiation Oncology, and Society of Surgical Oncology focused guideline update. Pract Radiat Oncol. 2016;6(6):e219–e34.
6. Hughes KS, Schnaper LA, Bellon JR, Cirrincione CT, Berry DA, McCormick B, et al. Lumpectomy plus tamoxifen with or without irradiation in women age 70 years or older with early breast cancer: long-term follow-up of CALGB 9343. J Clin Oncol. 2013;31(19):2382–7.
Acute and Late Skin Toxicity from Breast Radiation
Lindsey Sloan and Sara Alcorn
The Layers of Skin and Anatomy of the Breast
Composition of the Skin
An understanding of the anatomy and composition of the skin facilitates optimal assessment and management of radiation-related skin toxicity in the treatment of breast cancer. To review, the skin is comprised of the dermis and epidermis, the latter of which is further divided into five strata: corneum, granulosum, lucidum, spinosum, and basale [25]. An essential cellular constituent of these layers is the keratinocyte, which produces the primary scaffold protein of the epidermis, keratin. The maturation process for these cells is about 2 weeks [44], and complete reconstitution of the epidermis requires a period of 1–2 months [25].
Relevant to skin toxicity in the treatment of breast cancer, each epidermal layer has a unique function that can be disrupted during radiotherapy. The stratum corneum is the most superficial layer, and therefore, it is the foremost barrier to extrinsic pathogens. This layer is comprised of dead keratinocytes that have been pushed up from deeper portions of the epidermis during the maturation process. Beneath the corneum, keratinocytes within the stratum granulosum and lucidum mature and develop a strong keratin barrier. Langerhans cells are found within the next and thickest layer of the epidermis, the stratum spinosum [25]. These cells participate in antigen presentation, linking the cell-specific and innate immune response to pathogens. The highly proliferative keratinocytes of the stratum basale form the deepest layer of the epidermis. Here, melanocytes produce UV-protective melanin, and Merkel cells receive and relay superficial sensory information [25].
L. Sloan · S. Alcorn (*)
Department of Radiation Oncology and Molecular Radiation Sciences, Johns Hopkins University, Baltimore, MD, USA
J. L. Wright (ed.), Toxicities of Radiation Treatment for Breast Cancer, https://doi.org/10.1007/978-3-030-11620-0_2
L. Sloan and S. Alcorn
The epidermis rests upon the dermis, a fibroblast-dominated, blood-rich area important to thermoregulation. The dermis functions as the systemically integrated hub of the integument. Vital components of the dermis include lymphatic vessels, sebaceous glands, nociceptors, tactile receptors, and hair follicles. In times of repair, the dermis is a source of tissue fibroblasts and peripheral immune cells recruited from the local vasculature [27].
Breast Anatomy
The mature breast is comprised of glandular and adipose tissue extending from the second to the sixth intercostal space of the anterior and anterolateral chest wall [23]. Typically, it is bordered medially by the sternum and laterally at the midaxillary line, with the tail of Spence projecting into the axilla [23]. In most women, the breast naturally forms two regions susceptible to skin-to-skin contact: the inframammary and axillary folds. These folds are closely monitored throughout the course of breast radiation.
The skin of the breast uniquely contains underlying fibrous suspensory ligaments of Cooper, which connect compartments of the breast tissue to overlying skin [27]. This ligament-skin relationship is the reason that some breast cancers may produce an altered breast contour.
In non-pendulous breasts, the nipple is positioned around the fourth intercostal space [23]. It is surrounded by the areola, which receives oily secretions from the specialized areolar sebaceous glands [94]. Whereas the majority of breast skin rests on subcutaneous tissue, a layer of smooth muscle is found beneath the nipple and areola [94]. This smooth muscle aids in milk expression, as the lactiferous ducts from the glands below join and open at the nipple [23].
The innervation of the skin of the breast—and therefore the sensory relay for skin injury—involves small cutaneous branches of the nerves of the upper and midthorax. Individual variation is recognized within the literature; however the anterior cutaneous branches of the first through sixth intercostal nerves, the lateral cutaneous branches of the second through seventh intercostal nerves, and the supraclavicular branch of the superficial cervical plexus have been reported to supply the skin of the breast [41, 94].
Radiotherapy-Related Skin Toxicity in Breast Cancer
General Principals of the Radiation Response and Breast-Specific Considerations
In the management of breast cancer, therapeutic radiation is directed at targets including the whole or partial breast or chest wall, with or without coverage of regional lymph node regions at risk. The basic underlying mechanism of
Acute and Late Skin Toxicity from Breast Radiation
radiotherapy involves the generation of free radicals and the development of reactive oxygen intermediates that interact with cellular macromolecules, including nucleic acids like DNA [69]. A secondary wave of indirect damage to irradiated tissue occurs by resident cells from surrounding tissue and infiltrating immune cells from the vasculature. Both pro-inflammatory and repair-focused factors are secreted into the injured tissue, starting the recovery process [64]. Small amounts of radiation are delivered in daily fractions over a few to several weeks, often via tangent beams. The accuracy of the general biological response described above in the context of multi-fraction treatment is not clear. Skin toxicity may be due to the combined effects of new, daily injury by each radiation fraction, as well as through the secondary inflammatory response.
Acute Skin Toxicities
Acute skin reactions are experienced by up to 95% of patients undergoing radiation treatment to the breast [31, 59]. Radiation dermatitis is the general term used to describe a wide spectrum of skin toxicity, ranging from mild erythema to desquamation to rare tissue necrosis. Although patient-to-patient variability does exist, acute toxicities generally start around the 2nd to 4th week of radiation treatment [31]. By definition, acute skin toxicities occur within 30 days from completion of therapy. The maximal peak response occurs 1–2 weeks following the conclusion of radiotherapy [25].
Diagnosis and Grading of Acute Skin Toxicity
Acute radiation toxicities are diagnosed clinically, often at evaluation visits during the treatment course. Important to the diagnosis, formal assessment systems have been developed to evaluate patient skin toxicity. While a few standardized systems are routinely used, some trials have developed their own grading systems. Such variability in toxicity grading can complicate comparisons between studies and across interventions [35].
The Common Terminology Criteria for Adverse Event (CTCAE), Version 5, published by the National Institutes of Health, is probably the most commonly used acute toxicity scoring system. The CTCAE scores “dermatitis radiation” as the amount of desquamation and erythema that develops acutely from treatment [55]. The Radiotherapy Oncology Group (RTOG) acute radiation morbidity scoring criteria have five subcategories rating erythema and general dermatitis [18]. Highlighting the heterogeneity of dermatologic responses to radiation, the acute toxicity scale developed by Wright et al. describes six categories of acute skin reactions: “faint or dull erythema and/or follicular reaction and/or itching; bright erythema and/or tender to touch; dry desquamation with or without erythema; small or moderate amount of wet desquamation; confluent moist desquamation; and ulceration, hemorrhage, and/or necrosis” [91].
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As skin-related side effects have been demonstrated to affect quality of life, scoring systems such as the Functional Assessment of Cancer Therapy-Breast (FACT-B) and European Organization for Research and Treatment of Cancer (EORTC) QLQ-C30 have been developed to quantify this important aspect of skin toxicity [12, 72, 78].
Grading systems that include patient-reported outcomes have also been developed but are less frequently cited in the literature. The Radiation-Induced Skin Reaction Assessment Scale (RISRA) is similar to the provider-reported acute scoring systems but is completed by the patient undergoing radiotherapy [56].
Clinical Findings of Acute Radiation Toxicity
Erythema
Erythema starts as an asymptomatic flushing of skin that is exposed to radiation. It is considered one of the mild acute side effects and is estimated to be experienced by 90–95% of patients undergoing radiotherapy [59]. While it may occur a few to several hours after the first radiation treatment [42], it is unusual for erythema to be present prior to the delivery of 2000 cGy [46]. This flushing is presumably due to capillary dilatation in the affected area from to local release of vasoactive soluble factors [48].
An early form of erythema specifically affecting hair follicles is called follicular erythema. The RTOG acute radiation morbidity scoring criteria identifies follicular erythema as a grade 1 skin toxicity [18]. This toxicity is believed to occur early in treatment, as hair follicles have an intrinsic sensitivity to radiation [44, 51].
Skin erythema can be progressive and may persist for weeks. After the initial period of color discoloration due to quick-acting local factors, persistent erythema may be due to obstruction of arterioles by fibrin thrombi [48]. The RTOG acute grading system of skin toxicity identifies grade 1 side effects as asymptomatic erythema and grade 2 toxicity as erythema with itching [18]. Tools to measure erythema such as colorimeters and spectrophotometers have been developed but are not regularly used within the clinical setting [11, 70]. Notably, erythema heralds future desquamation.
The Desquamation Continuum
The term desquamation describes a wide range of radiation injury that is commonly encountered during and after treatment. It is the consequence of radiation injury to both the maturation process and the proliferative capacity of keratinocytes [53]. By the CTCAE acute toxicity grading scale for radiation dermatitis, dry desquamation is a grade 1 sequela [55]. Early sebaceous gland impairment from treatment leads to scaling and itching of the skin, resulting in dry desquamation. This grade of toxicity is identified in about half of patients undergoing external beam radiotherapy [5, 14].
Dry desquamation may progress to more severe injury, such as moist desquamation. Moist desquamation is characterized by weeping and loss of the epidermis and is used as a metric of more serious skin toxicity [31]. CTCAE grade 2 radiation dermatitis includes moist desquamation limited to the skin folds, and grade 3 encompasses moist desquamation occurring in non-creased areas that bleeds easily [55]. Moist desquamation occurs in 15–48% of patients with breast cancer receiving radiotherapy [25].
Rarely, desquamation can progress to necrosis and ulceration. Grade 4 toxicity by the CTCAE acute grading system represents dermal injuries that regularly bleed and may require treatment with skin grafting [55].
Late Skin Toxicity
Late skin toxicity is defined as side effects of treatment that occur one to 3 months following radiotherapy. Like acute toxicities, these can range from mild to significantly bothersome; thus, these outcomes should be considered as important factors relative to maintaining quality of life after treatment.
Diagnosis and Grading of Late Skin Toxicity
As with acute toxicities, grading systems for late toxicities are also available. One assessment scale used for evaluating late fibrosis and atrophy is the RTOG/ EORTC Late Radiation Morbidity Scoring Schema for subcutaneous tissues [18]. In addition to acute toxicities, the CTCAE includes scoring for late effects as well.
Types of Late Skin Toxicity
Radiation-Induced Fibrosis
Radiation-induced fibrosis, or a thickening or hardening of skin with or without associated pain, is one of the more common late sequelae of radiotherapy [25]. Histopathologically, fibrosis is described as a marked abundance of fibrous scar tissue within the dermis [25]. As with other fibrous scarring processes, radiationinduced fibrosis is believed to be mediated by transforming growth factor beta (TGFβ) [15]. The RTOG/EORTC Late Radiation Morbidity Scoring Schema for subcutaneous tissue evaluates fibrosis on a scale from 1 to 5, with grade 1 toxicity described as slight induration or fibrosis, grade 2 as moderate but asymptomatic fibrosis with slight field contracture and less than 10% linear reduction, and grade 3 as significant induration with field contraction and greater than 10% linear reduction [18].
L. Sloan and S. Alcorn
Atrophy
Atrophy related to radiation treatment is identified as a thinning of the subcutaneous tissue within the treatment field. The RTOG/EORTC Late Radiation Morbidity Scoring Schema for the skin evaluates atrophy on a scale from 1 to 5, with mild, non-confluent, and significant atrophy comprising grades 1, 2, and 3, respectively [18]. The CTCAE scores based on distribution of skin changes and incorporates changes in skin quality as well [55].
Hyperpigmentation
Hyperpigmentation within the radiation treatment field results from skin melanocyte activation. This side effect may occur acutely but may also persist and progress following treatment. Hyperpigmentation is graded by the CTCAE based on the distribution or social impact of the darkening, with grade 1 covering less than 10% of the body surface area without psychosocial impact to the patient and grade 2 covering more than 10% body surface areas or with associated psychosocial impact [55]. Rarely, hypopigmentation may occur in radiation-induced vitiligo, which may be immune cell-mediated [84].
Telangiectasia
Telangiectasias are found as a late and progressive complication of radiation toxicity. These vascular aberrations represent dilated blood vessels close to the skin surface that may be cosmetically bothersome to some patients. The pathophysiology may involve overexpression of platelet-derived growth factor [21]. RTOG grade 1 skin toxicity includes pigmentation change, grade 2 toxicity identifies moderate telangiectasia, and grade 3 involves significant telangiectasia [18]. As with hyperpigmentation, CTCAE classifies telangiectasias as grade 1 if covering less than 10% of the body surface area and grade 2 if covering more than 10% of the body surface area, with psychosocial impact [55]. Telangiectasia is also included in the description of CTCAE grade 1 skin atrophy [55].
Morphea
Morphea is described as a localized scleroderma condition, distinct from radiation fibrosis [25]. It is estimated that 2 in 1000 patients develop this toxicity following breast radiation [8]. Morphea is marked by a thickening of the skin, often causing noticeable retraction [22]. As in some cases of scleroderma, patients develop localized red or pale dermal plaques. It may develop weeks to years after initial radiation treatment [85]. Unlike hyperpigmentation and telangiectasias, such plaques may extend outside of the radiation field, perhaps due to systemic T cell dysfunction in
Acute and Late Skin Toxicity from Breast Radiation
affected patients [85]. Alternatively, the pathogenesis of morphea may be similar to radiation-induced fibrosis and attributable to an overactive TGFβ pathway [1]. However, unlike radiation-induced fibrosis, morphea is less clearly associated with dose and severity of acute skin toxicities [17].
Radiation Recall
Radiation recall reaction is characterized as a dermal inflammatory response within the radiation field in reaction to a pharmaceutical. By definition, it occurs a few to several weeks following radiotherapy and resolves with cessation of the offending agent [55]. Symptoms of the entity are similar to that of radiation dermatitis; as such, the CTCAE grading for these two toxicities is identical [55]. Radiation recall has generally been reported as an overexaggerated dermal response to chemotherapy and antihormonal therapy including tamoxifen and trastuzumab, but other pharmaceuticals such as fluoroquinolone antibiotics have been identified as potential causative agents [9, 29, 54, 63, 88].
The incidence of radiation recall may vary by the modality of radiation delivered. For example, in a clinical trial investigating the use of MammoSite brachytherapy, radiation recall was reported in 18% of patients treated with this device [ 30 ].
Risk Factors for Acute and Late Radiation Skin Toxicity
Both patient- and treatment-related factors are believed to play a role in the development of skin toxicity after radiotherapy for breast cancer.
Patient Predisposition to Skin Toxicity
Patient Characteristics
Many studies have investigated patient-related factors that may contribute to the development of skin toxicity in breast radiotherapy. Increased age and smoking have been associated with higher risk of skin toxicities including telangiectasias and radiation-induced fibrosis [47, 52, 62, 76]. Elevated body mass index and patient weight have been associated with adverse outcomes such as development of moist desquamation in both prospective trials and retrospective studies [4, 19, 47, 49, 58, 62]. Perhaps as the confluence of larger breast size, greater body mass, and higher disease stage, larger treatment field size is also related to increased risk of development of radiation skin toxicity [4, 19, 24, 49, 62, 92].
Individuals that tend to complete repeated movements such as in running may be at higher risk for radiation dermatitis [44]. Interestingly, Noh et al. found that at one
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center, women treated in the morning had less skin reactions than the afternoon [57]. This may be explained by social behaviors, including administering creams and lotions in close proximity to the time of treatment. Alternatively, more complex biological explanations may exist.
Genetic Predisposition via Altered DNA Damage Repair
Individuals with impaired DNA damage pathways have been reported to be at a higher risk of skin toxicity. ATM is a protein that is involved in repair of doublestranded DNA repair breaks, such as those that occur from radiation injury. Individuals with ataxia telangiectasia, an autosomal recessive syndrome due to germline mutations in ATM, are known to demonstrate marked radiation sensitivity [16]. More commonly, individuals may be heterozygous for ATM mutations, which is suspected to occur in 1% of the population [37]. In a study investigating patients with breast cancer that experienced serious late radiation toxicities, mutations within both copies of the ATM gene were associated with increased risk of toxicity [38]. Ho and colleagues found increased rate of all grades of late toxicity in patients with breast cancer who were heterozygous for the G5557A variant ATM sequence [33]. Similarly, Andreassen et al. identified increased risk of skin toxicity in patients with the N1853D variant [2]. Other gene mutations within DNA repair pathways have been identified, but corroborative studies associating these variants with radiation toxicities are lacking.
Dysfunctional Immune Response
As previously noted, the immune response may be important in both the acute immune reaction to radiation and late effects from smoldering inflammation. Unsurprisingly, alterations in immune activation and regulation have been associated with development of higher-grade radiation-induced skin toxicities. For example, the presence of the endothelial synthesize nitric oxide (eNOS) G874T polymorphism is associated with heightened levels of oxidative stress; patients with this polymorphism have been reported to have an increased rate of acute skin toxicity following breast radiotherapy [80]. Supporting the importance of an intact reactive oxygen management system, increased ARG1 mRNA level is also associated with development of acute skin toxicities [43]. Highlighting the systemic impact of radiotherapy, biomarkers such as elevated levels of high-sensitivity C-reactive protein have been linked with an augmented risk of grade 4 skin toxicity after initiation of breast radiotherapy [36]. Specifically for fibrosis, a polymorphism within the gene for TGF β 1, T869C, was found to be significantly associated with development of grade 2 and 3 toxicity [79]. The presence of comorbid autoimmune diseases such as scleroderma has been a concern for exaggerated side effects; however, one recent retrospective study reported that half of patients with scleroderma did not have a dermatologic flair in following treatment [73].
Radiation Delivery and Planning Risk Factors
Many current radiation protocols do not specify the skin as a dosimetric region of interest. As such, in clinical practice, skin dose is often approximated by dose measured at the patient surface. To better characterize radiation dose to the skin, the International Commission on Radiological Protection suggests that skin dose be determined as the radiation dose at 0.07 mm from the skin surface, roughly aligning with the stratum basale [39].
Several dosimetric factors have been linked to skin outcomes. For example, higher total prescription doses with and without surgical bed boost are associated with increased risk of skin toxicity [61, 62]. Dose inhomogeneity of >107% of the prescribed dose and increasing volumes of tissue receiving 107% and 110% of the prescribed dose have all been shown to be associated with worse skin outcomes [15, 83]. The use of bolus to augment superficial dose has been associated with increased risk of radiation-induced fibrosis [6, 82, 91]. Similarly, the inframammary and axillary folds act as self-bolus, resulting in higher skin doses and subsequent development of localized skin toxicity at these sites [31]. Indeed, Yang and colleagues found that axillary fold dose is an important dosimetric predictor of skin toxicity during whole breast irradiation [93].
Fractionation also appears to have significant implications for development of skin toxicity. Both retrospective and prospective studies have reported that moist desquamation is more common in conventionally fractionated as compared to hypofractionated breast radiotherapy [3, 58, 74, 92]. Moreover, a randomized clinical trial found lower rates of dermatitis, pruritus, and hyperpigmentation in patients treated with hypofractionated versus conventionally fractioned plans [74].
Further, treatment intent and delivery modality may affect incidence of skin toxicity. Inclusion of regional nodal fields has been found to portend a higher risk of moist desquamation [58, 92]. In one report, brachytherapy-based accelerated partial breast irradiation was found to increase the rate of developing telangiectasias as compared to whole breast irradiation (14.4% vs. 2.9%) [90]. A number of studies have shown that patients receiving intensity-modulated radiotherapy (IMRT) for breast cancer experience less moist desquamation as compared to those treated with 3D conformal techniques [19, 59]. This may be attributed to the multiple beam angles used in IMRT, possibly resulting in a relative skin-sparing effect due to fewer monitor units delivered in a path directly tangential to the patient surface [40].
Other Non-radiation Treatment Characteristics
Breast cancer management strategies employed prior to delivery of radiotherapy have been reported to increase the risk of radiation-related skin toxicity. Specifically, history of surgical intervention and larger resection volumes [4] and receipt of chemotherapy prior to radiation are associated with a higher risk of the developing subsequent radiation dermatitis [19, 31, 58]. Particular chemotherapeutic agents have been identified as especially problematic, such as Adriamycin in patients receiving accelerated partial breast irradiation [87].
L. Sloan and S. Alcorn
Management of Acute and Late Skin Toxicity
Management of Acute Toxicity
Despite the high incidence of acute toxicities following breast radiation, available evidence for side effect management is limited to small studies or clinical trials focused on efficacy of new therapeutics. Available strategies include interventions that are either proactive against or reactive to toxicities developing over the course of radiotherapy and recovery.
Prevention of Acute Skin Toxicity
Anticipatory practices employed at the initiation of radiotherapy may delay or avoid the appearance of high-grade skin toxicities [44]. These include behavioral practices and topical agents.
Prior to beginning radiotherapy, behavioral factors should be reviewed to identify potential habits and lifestyle activities that could increase the risk of skin toxicity. Considerations include the following:
• Smoking cessation should be strongly recommended [25].
• Physical activities that irritate the skin within the radiation field should be avoided or pursued with caution, including repetitive arm motions as in running [25].
• Although there is a tendency to discontinue use of supportive undergarments due to discomfort, patients should be encouraged to wear such undergarments in an effort to avoid friction [51].
• General hygiene practices should be explored and optimized. In two randomized trials comparing washing with soap versus washing with only water in women undergoing breast radiation, there was no excess toxicity with the addition of soap [13, 68]. Based on these studies, it is recommended that women undergoing radiotherapy should continue to wash the treated area with non-perfume soap [25]. The use of deodorant during radiotherapy is controversial, as there is concern that the metallic ingredients within some deodorant could lead to scatter and increased skin dose. Four studies investigating toxicity outcomes in patients that either used versus omitted use of deodorant have failed to show a significant increase in skin reactions with use of these products [7, 26, 81, 86].
The role of topical agents in the prevention of radiation-related skin toxicity has also been investigated. The goal of these prophylactic approaches is to moisturize the affected skin, reduce friction [25], and possibly minimize local inflammation. Yet results regarding the efficacy of specific products are often conflicting. For example, whereas one randomized study of calendula cream showed a significant decrease in acute dermatitis with this agent, another report found no appreciable benefit [60, 75]. Similarly, the benefit of aloe in the prevention of skin reactions is unclear. While randomized and non-randomized studies have shown both benefit and no benefit to this agent as a preventative strategy [25, 35, 89], the preponderance of evidence seems to suggest that aloe is ineffective at significantly decreasing
Acute and Late Skin Toxicity from
of the incidence of desquamation. Use of oil emulsions has generally been discouraged as they could theoretically increase the dose to the skin by creating pseudobolus. However recent clinical trials have not confirmed this association [45, 65]. As the sum of available literature, a systemic review by the Cancer Care Ontario’s Supportive Care Guidelines Group (SCGG) did not find sufficient evidence to support or refute the use of a particular topical agent [10].
The role for topical steroids for toxicity prevention has also been investigated. Boström et al. reported that the combination of mometasone furoate and emollient care was found to result in less acute radiation dermatitis by visual skin scoring and spectrophotometry as compared to emollient alone [11]. A follow-up double-blind randomized study confirmed that mometasone furoate demonstrated a decrease in RTOG acute radiation morbidity scoring criteria, with an increase in quality of life also measured [32]. An additional randomized, double-blind investigation of mometasone furoate vs. Eucerin cream for patients receiving postmastectomy radiotherapy also reported decreased rates of moist desquamation, lower incidence of maximal skin toxicities, and delayed time to development of grade 3 dermatitis for the mometasone furoate arm. Of note, there was no difference in patient-reported skin outcomes between treatment groups in this study [34].
Given the range of conflicting evidence noted, the SCGG consensus recommendations support the use of a non-scented and lanolin-free hydrophilic cream for potential prevention of radiation skin reactions [10]. Other agents are being explored in clinical trials to prevent the development of acute skin toxicity including creams targeting TGFβ [15].
Treatment of Acute Skin Toxicity
After the appearance of skin changes in radiation treatment, it is recommended that patients continue to use their daily topical cream [25]. One goal is to increase skin moisture in an effort to support regeneration of the epidermis [44]. Products that support this aim include Mepilex dressings and hydrocolloid and hydrogen dressings. Silver ion-based creams may be applied if there is concern for infection [25]. The SCGG recommendations also support the use of low-dose topical steroids for the management of pruritus and irritation [10].
Rarely do patients require oral pain medications, as topical approaches are typically effective in decreasing the pain or discomfort experienced. In the most severe form of skin damage ulceration and necrosis, surgical intervention with skin grafts and flaps may be required [77].
Treatment of Late Toxicity
Fibrosis is a common late consequence of breast irradiation. However, treatment options are limited. Pentoxifylline, a phosphodiesterase inhibitor, has been reported to block TGFβ production and may lead to the regression of superficial radiationinduced fibrosis [20].
L. Sloan and S. Alcorn
Due to the nature of suspected pathogenesis of morphea, treatment strategies have included immune modulators. Yet most evidence regarding the management of this entity is based on case reports and experiences from non-radiationinduced morphea. Oral and topical steroids may be considered [ 71 ]. Others have had success with psoralen UVA (PUVA) therapy and ultrasound phonophoresis combined with hyaluronidase [ 28 ]. Topical calcipotriol, a vitamin D3 analog, and UVA1 irradiation have demonstrated efficacy in treating other forms of morphea [ 1 ].
Telangiectasia may be treated with pulse dye laser. Small cohort studies have showed benefit in both quality of life and cosmetic appearance from this strategy [50, 66, 67].
Considerations for Including Risk of Toxicity in Management Decisions
With modern management strategies, many breast cancers can be approached with curative intent and the probability of excellent, durable disease control. Because skin toxicity has been demonstrated to affect patient quality of life [3], accurate description of adverse risks as well as thoughtful and proactive management of skin toxicity should be employed as a means to support favorable long-term skin outcomes. While most patients will experience only grade 1–2 skin toxicities, these considerations are particularly important among patients with numerous genetic, behavioral, and treatment-specific risk factors for the development of more severe adverse skin outcomes.
Conclusions and Future Directions
Skin toxicity is a common side effect of radiotherapy to the breast, and it has significant implications for patient quality of life. While growing evidence may allow us to better identify patients at risk for radiation-induced skin reactions, we are outfitted with few reliable tools to assess, prevent, and treat the toxicities we predict. Moreover, available tools remain relatively subjective and are not consistently employed in clinical practice or even across prospective protocols. Such tools cluster skin sequelae of differing histopathologic and immune etiology under umbrella terms such as “radiation dermatitis.” This may hinder our ability to isolate and study specific subtypes of skin reaction. Thus, important next steps include the development of comprehensive skin toxicity grading systems and instruments to characterize and diagnose the range of skin response to radiation. By encouraging adoption of such optimized assessment tools and fostering understanding of skin sequelae as individual entities, we may be able to improve toxicity outcomes for future patients.
References
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L. Sloan and S. Alcorn
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him that we had a cavalry fight a couple of weeks before at Bardstown, where no doubt his boys were engaged, when on his further enquiry about the engagement, I told him how we scattered them all over the country, killing and wounding a great many. The ladies burst into tears and went back into their room, and the old man had nothing more to say about his boys.
I then again tried to persuade him to give us at least one wagonload of bacon, promising him that if he would send his team and a boy to drive it to Lebanon, he would surely have them returned, when he again refused in a spiteful, insulting manner. I told him that we had understood he had some six or eight yoke of workoxen and in Texas we knew all about handling oxen and we would go into his pasture and drive them up and hitch them to the wagons that were at the house, but this was only a threat. We gave him up as a bad job and when we reached the pike about three miles from there, we met a citizen who told us that Wheeler’s cavalry had evacuated Lebanon and burnt all the meat stored there, which we were induced to believe, and decided to ride back to the Harrodsburg Pike and get with our command, which we did.
Our army then continued to retreat, the main part of the army moving towards Crab Orchard, where we struck the Cumberland Gap road, while the army, under Kirby Smith, was struggling over Big Hill, and had still to join the main army at the junction of the roads at Pitman’s. The army then moved into the mountains on the Cumberland Gap road, which, owing to the character of the country, was generally restricted to a single wagon track. This stretched out our columns of retreat for perhaps twenty miles or more and cut up the road very badly, frequently causing wagons to stall. Two infantrymen consequently were detailed with every wagon, of which we had thirty-eight hundred, laden with provisions and valuable stores. This detail of two with each wagon was ordered to assist any wagon that was stalled by taking hold of the wheels, thereby helping the team to pull the wagon out of the rut.
A division commander was detailed every day to take charge of the wagon train and artillery and keep it moving. When a wagon stalled, the whole line of retreat, infantry, wagons and artillery behind
it, would have to wait until it would move again, thereby seriously impeding our line of march and causing the cavalry in the rear desperate fighting sometimes to hold off the enemy.
It was reported of General Cheatham, when he had charge of the train, that one of his wagons was stalled, and he put spurs to his horse and rode up the line and reached the wagon. The driver was whipping his mules and the two infantrymen were standing by the roadside, resting on their guns. At the sight of this, he jumped off his horse, took hold of the spokes of the wagon wheel and tried to turn it, but all to no purpose. The two guards still stood resting on their guns. General Cheatham lost his patience and turned around and slapped one of the guards in the face. This happened to be an Irishman, who said, “Be God; if you were not Gineral Cheatham you couldn’t do this.” General Cheatham pulled off his sword belt, coat and hat and threw them down by the side of the road and said, “Now, there lies General Cheatham and here is Frank Cheatham; now light in.” They say that at this invitation the Irishman lit in and got the best of the bargain, of which General Cheatham never made any complaint. The two men then took hold of the wheels in conjunction with General Cheatham, and started up the wagon, and with that the whole line of retreat.
This incident was currently reported and generally believed by all who knew General Cheatham, but I would not be willing to vouch for the same, as it is almost past belief.
After leaving Crab Orchard, General Buell dispensed with his cavalry, as they were unable to cope with ours and moved only with his infantry and artillery in advance. To enter into the details of the rest of this campaign, would require too much space and will only say that the brigade of General Wharton, which always includes the Terry Rangers, in conjunction occasionally with other cavalry, were expected to and did succeed in retarding the pursuit of the enemy, restricting his advance to from six to eight miles a day only, thereby protecting our infantry column, as well as the artillery, ordnance and thirty-eight hundred wagons loaded with valuable army stores. On this retreat the infantry were called on only one time to fire a gun. We met the enemy in a general engagement at Mount Vernon, Barren
Valley, Rocky Hill, Bushy Mound, Wild Cat, Pitman’s Road, Little Rock, Castle River and many other points, inflicting on them considerable loss. This mountain service on the part of the Rangers proved a most severe tax on their endurance, on account of being deprived of rations. At one time, for nearly two days, we depended on picking up raw corn left in the camps of artillery and wagons, where the horses and mules had been fed. A number of times, after fighting all day long, we had to go out into the hills ten or twelve miles to find forage for our horses before we could retire to get a little rest. Our camping places were frequently by the light of the enemy’s fires.
To give the reader a better idea of the valuable service we rendered, I will quote an order issued by General Wheeler, read to us at Cumberland Gap, October 23, 1862.
GENERAL ORDER NUMBER THREE:
“Soldiers of the Cavalry Corps, Army of Mississippi:
“The autumn campaign in Kentucky is over, your arduous duties, as the advance and rear guard, for the present, are finished. Your gallantry in action, your cheerful endurance in suffering from hunger, fatigue and exposure, render you worthy of all commendation. For nearly two months you have scarcely been for a moment without the range of the enemy’s musketry. In more than twenty pitched fights, many of which lasted throughout the day, you have successfully combated largely superior numbers of the enemy’s troops of all arms. Hovering continually near the enemy, you have engaged in no less than one hundred skirmishes. Upon the memorable field of Perryville, alone and unsupported, you engaged and held in check during the entire action, at least two infantry divisions of the opposing army. By your gallant charges on that day you completely dispersed and routed a vastly superior force of the enemy’s cavalry, driving them in confusion under their artillery and infantry supports, capturing in hand-to-hand conflicts many prisoners, forces and arms. Your continuous
contact with the enemy has taught you to repose without fear under his guns, to fighting wherever found and to quietly make your bivouac by the light of his camp fires. On this continued series of combats and brilliant charges, many great men have fallen. We mourn their loss. We commend their valor. Let us emulate their soldierly virtues.
“JOSEPH
WHEELER, “Chief of Cavalry.”
CHAPTER XVII.
O P C
After leaving Cumberland Gap our army again moved into Middle Tennessee, with headquarters at Murfreesboro. Our cavalry in the advance camped near La Vergne, at Nolandsville and Triune. The enemy concentrated at Nashville, from whence they sent out foraging parties, supported by large infantry forces with which we had daily engagements, restricting their foraging within a small area of country. At Nolandsville, where General Wharton made his headquarters, we camped nearly a month, when Lieutenant Decherd was instructed to select about fifteen men and cross the Cumberland Mountain, for the purpose of buying fresh horses, which were very much needed. I was ordered to go with this party.
While camped near Winchester, Tennessee, intending to cross the mountain the next day, we heard the distant roaring of the guns of the battle of Murfreesboro, which was not expected so soon when we left the command, and which proved a great disappointment to our party, as we felt that every man was needed for such an event. We, therefore, hastened back to the army, which we found evacuating Murfreesboro, and reported. Of the Rangers’ part in that great battle I will not mention in this, as that is of record in the general reports of General Bragg and others, and will only say that they fully sustained their character as one of the leading regiments in this army, capturing prisoners, artillery, wagon trains, etc., and finally covering the retreat of the army off the field.
Our army then continued its retreat through Shelbyville to Tullahoma, our cavalry still operating on the north side of Elk River. Before crossing Elk River a courier reached General Wheeler from General Forrest, after Wheeler had crossed the bridge, requesting him to hold the bridge until he (Forrest) could cross with his
command. Promptly on receipt of this information, General Wheeler, with a portion of his command, notably the Fourth Alabama Cavalry, recrossed the bridge to the north side, determined to hold the same until General Forrest had crossed with his command. Before Forrest reached Shelbyville, however, General Stanley, with a heavy force of cavalry, outnumbering Wheeler’s little force ten to one, charged and forced them back across the river, cutting General Wheeler off from the bridge. General Wheeler spurred his horse to the bank and over it, into the dangerous river, which had been swollen by excessive rains, making a leap of not less than twenty feet, with Stanley’s cavalry shooting after him and continuously firing on him until he reached the opposite bank. This was, perhaps, the most miraculous escape he had during the war.
Before reaching Tullahoma, a Captain Gordon, who had distinguished himself near Bardstown, where he held in check a whole brigade of the enemy’s infantry on the Bloomfield Road for a whole day with only twenty men, was ordered to select twenty men from the Rangers and enter Kentucky, for the purpose of gaining information of the disposition of the enemy’s forces, preparatory to a general raid by our cavalry. The history of this trip, which resulted in my being wounded and captured and held a prisoner just one year, lacking a day, I have already recorded, and by an oversight, it crept into this history ahead of the proper time.
Recurring to the hard service sustained by us in the mountains between Crab Orchard and Cumberland Gap: The last night we were on picket duty our company had dwindled down to seven men and I happened to be on vidette with a messmate, John Cochran. Just at daylight, when the enemy usually made its appearance, we were relieved by two others of the command and when we reached the reserve picket, discovering a grassy spot in the middle of the road, I told Cochran I must try to steal a little nap, and laid down on this grassy spot, holding my horse by the bridle, when I was awakened, only about ten minutes after, by Cochran stooping down from his horse and jabbing me with his pistol. The reserve picket had formed a line across the road, just a little back of where I was sleeping and were firing on the enemy’s advancing skirmish line, the noise of
which failed to awake me and it was only his prodding me with the end of his six-shooter that got me awake. I had just time enough to swing on to my horse and get out of there. Here Cochran’s prediction, frequently made, that he would bet Graber would wake up some fine morning with a Yankee bayonet sticking in him, came very near being verified. I merely mention this to give the reader a fair idea of our complete exhaustion for the want of sleep, continuous hunger and arduous duties.
CHAPTER XVIII
G J ’ F
S —S
Recurring to my service in Captain Britton’s company, acting as escort to General Hood at Dalton, Georgia, where I described the meeting of the several generals with General Hood at his headquarters in the rear of Railroad Gap: On our return to camp that night after supper, Captain Britton suggested he should go up to headquarters and pump Major Sellars on the meaning of the meeting that morning. He reported on his return from a visit to headquarters that General Mower, commanding Hooker’s old corps, had moved down to Snake Creek Gap during the day, which was located about nineteen miles in our rear and about ten miles west of Dalton.
General Hood plead with General Johnston that morning for permission to move out of his works through Railroad and Rocky Face Gaps with his corps and defeat Sherman’s Army before Mower could return to reinforce them. Captain Britton said that he would bet our army would be in full retreat that night, falling back to Resaca, which prediction was verified, as, by daylight next morning, our infantry and artillery were engaged with the enemy at Resaca, where we came very near losing a large part of our army by having their retreat cut off.
Had General Johnston yielded to General Hood’s plan, there is no question but what he could have destroyed Sherman’s Army; here was a golden opportunity lost by General Johnston, and was the beginning of the downfall of the Confederacy.
After about two weeks I succeeded in getting a horse with the regiment and continued with the regiment during the whole of the North Georgia campaign, the details of which I will not venture to
insert, as they will be recorded fully in a history now being written by Colonel Ben F. Weems of Houston.
During the siege of Atlanta General Sherman started out two cavalry expeditions, one under a General Stoneman to move around the right wing of our army, and one under General McCook around the left wing of our army, both to unite on the Macon line of railroad, and to destroy and tear up the same, then move on to Andersonville and release our prisoners. Had these expeditions proven a success, with an army of probably twenty-five or thirty thousand released prisoners turned loose in our rear, it would have wound up the Confederacy. At Atlanta, General Hood took command of our army, not exceeding thirty-six thousand muskets and, to use his words, “This army through General Johnston’s retreating from Dalton, had become an army of laborers by day and travelers by night,” while the army at Dalton, including Polk’s corps at Rome, numbered eighty-six thousand muskets, and was better equipped and organized than any army the West had ever had. The North Georgians and Tennesseans, largely constituting this army, with their families inside of the enemy’s lines, were anxious and eager for an advance, and there is no question of doubt had General Hood been permitted to give battle at Dalton, our army would have recaptured Tennessee and Kentucky.
Referring back to the enemy’s cavalry expedition out of Atlanta: General Stoneman, with a large part of his force, and a lot of convalescents in the town of Macon, Georgia, were captured near Macon by General Iverson, commanding Georgia cavalry. General Wheeler with our brigade, Ross’ and Roddy’s, forced McCook to a general engagement on the evening of the second day between Noonan and Philpott’s Ferry, where they finally surrendered, with the exception of himself and staff, and Colonel Brownlow and some other line officers, who swam the river that night and made their escape.
General Wheeler issued an order that night for no man to cross the river after these fellows, when I, with several of our regiment, decided there must be some mistake about it and crossed the river to try to catch these fellows, specially anxious to capture Colonel
Brownlow Immediately after crossing the river we found a quartermaster’s clerk, so he represented himself to be, left wounded at a house. His wound, however, was not very serious we thought. He had on a magnificent pair of boots, which just about fitted me and I had been unable to secure boots, only wearing shoes, when I proposed to him to exchange with me, which he readily did. While he was pulling off his boots, the lady of the house came in and opened a tirade of abuse on me for taking a poor, wounded man’s boots. I told her I had but just come out of a Federal prison where they treated us worse than that and I was satisfied that my shoes would prove more comfortable to this man at Andersonville, than the boots, to which our prisoner agreed. We then continued our pursuit on the main road to Wedowee, the county seat of Randolph County, Alabama, occasionally taking a prisoner, whom we would turn over to reliable citizens, to be taken to West Point where we had a garrison. We were unable to secure many prisoners, probably not exceeding eight or ten, as those afoot would hear us coming in the road and dart into the brush, while their officers impressed every horse they could lay their hands on and soon outdistanced us with their fresh horses.
At Wedowee we found a tanyard, where I purchased a lot of good leather, sufficient to rig a Texas saddle. We had some men detailed to make saddles, who were experts in such work and moved down with the army as fast as it retreated. Our first shop was at Ackworth, Georgia, where they did a good deal of work, but were prevented from turning out anything extensive ever after, for the reason they were unable to get leather. I paid one hundred and twenty-five dollars for the leather I got at this tanyard. Colonel Harrison promised me, after my return from prison, that if I would furnish the leather he would have rigged for me one of the finest saddles that could be made, which was the inducement for me to carry this roll of leather on my horse’s back.
Going back into the town from the tanyard, we stopped at a hotel to get some dinner. This was one of the ordinary country hotels with a porch in front and large square columns under the porch. While eating dinner, I had a seat at the end of the table where I could see
out on the street. The hotel was located somewhat under the hill, away from the square, when I discovered Carter Walker, one of our party, who had finished dinner, behind one of the posts with his pistol out, talking to some one on the street towards the courthouse. Having his pistol out suggested to me that there was trouble ahead, so I jumped up and told the boys to come on. As we got out on the porch we discovered about fifteen or twenty men on their horses near the courthouse, with one of them talking to Carter Walker, about fifty yards distant from us. As soon as we came out, he retired and when he got back with his crowd, said something to them and immediately they wheeled and left town. This proved to be a party of bushwhackers, who were not anxious for a fight with us. We now decided to return and when a few miles from town, we heard of an old gentleman, whose name I have forgotten, the only Rebel citizen in that section, whom we decided to go and see and get some information from.
After reaching his house and getting acquainted, we decided, on his urgent request, to stay with him that night, as we were very tired, as were also our horses, and we did not suppose there was any great need for our services immediately after the destruction of the enemy’s cavalry. This old gentleman had had considerable trouble with his Tory neighbors, who came to his house several nights and opened fire on him, which he, his old lady and his daughter, a barefooted girl of eighteen, returned with their squirrel rifles through port holes cut in the logs of his house.
On the information of our old friend, we decided to visit the house of a Tory neighbor of his, across the mountain, who belonged to the Tory regiment in camp at Rome, which we did. Riding up to the house in blue overcoats, we called for a drink of water, when a lady invited us in, supposing that we were Federal soldiers. In our talk with them, there being two other ladies in the house, we represented that we were Federal spies on our way to Andersonville to make arrangements about the escape of our prisoners there, which created quite an interest with these women, who told us that a large number of young men of the neighborhood belonged to the First Federal Alabama Cavalry, stationed near Rome, and quite a number
of them were expected home pretty soon on a furlough. We then arranged with them to tell their boys about our visit and tell them that we expected to return there in about ten days, as we would probably need their assistance and we wanted to confer with them. Our idea was that we would return there at that time, with our company, and capture the whole outfit.
After making complete arrangements, we started back towards Philpott’s Ferry, where we again recrossed the Chattahoochie and, on our arrival at Noonan, found that Wheeler had moved over to Covington, on the Augusta road.
Riding all that day in a drizzling rain, we called at a house for the purpose of getting some feed for our horses and something to eat for ourselves. Night had already set in. We asked the gentleman if he could take care of us that night, give us a place to sleep on the floor, as we never slept in a bed, and get something to eat for our horses and ourselves. His answer was, “Certainly, gentlemen; light and come in.” I told him before we got off our horses that we were about out of money and did not have enough, perhaps, to pay our fare, when he stated that if his wife had anything left from supper we could have it and he would give us some shattered corn for our horses. We, of course, didn’t feel very comfortable under such liberality, but decided to stay, nevertheless, and sleep down in his barn, some distance from the house.
While we were waiting for his wife to gather what she had left from supper, he asked us if we were that command the other day that fired on the Federals when they were tearing up the railroad near his house. I told him that we were, and he said, “They were in my pasture trying to catch my horses, when they heard the guns fire and you ought to have seen those devils run.” When we went in to supper we found a little piece of cornbread and a little butter, all they had left from supper, so the woman stated, not enough to satisfy one man’s hunger. We did not sit down at the table, didn’t touch anything they had to offer us, and went down to the crib to get the shattered corn for our horses, which he consented for us to take, fed our horses and laid down to rest for the balance of the night. Next morning we got up early and without going to the house, proceeded
on the road towards Covington. Here now, was a fair illustration of the want of appreciation of a Confederate soldier, with a selfish lot of people, whom we occasionally met. Rest assured it was very discouraging to us. The idea of coming all the way from Texas to fight for and protect these people! He had told us that we saved his horses from capture by engaging the enemy near his house; you can imagine our disgust at such treatment. We now proceeded on the Covington road. When about two miles from there we came to a large, white house, a magnificent place, and rode up to the gate. A man about twenty-five years old, well dressed, wearing a white starched shirt, the first we had seen in a long time, came out to the gate. When within twenty feet of us, espying the leather on my horse’s back, tied to the rear of the saddle, he called out, “I want that leather.” I said, “If you need it any worse than I do, you are welcome to it.” He said he did, he wanted to make shoes out of it. I told him that I wanted to make a saddle out if it, to ride to keep Federals off of him, when he insisted that he needed it worse. I then told him that we wanted some breakfast and some feed for our hoses. He said, “All right, gentlemen; light and come in.” Before getting down I said, “I had better tell you that we are nearly out of money, not enough to pay for breakfast and feed, away from our command unexpectedly, but as soon as we get with them and we have an opportunity, we will send it to you.” He stated that he couldn’t afford to feed us without pay, that the armies had been around him for some time and had nearly eaten him out of house and home. I told him that he needn’t say anything more, that we didn’t want anything he had, although our horses were hungry, as well as ourselves. As we rode off he called after us, “I’ll feed you for that leather,” thus adding insult, but we decided not to notice him.
About three miles further down the road we came to another house, a somewhat humble cottage, and stopped to make some inquiry, when a lady came out to the gate and we asked how far down the road we could find a house where we could get something to eat for ourselves and feed for our horses. She asked us if we had tried at the big, white house we had passed on the road. We told her that we had and were refused because we had no money. She then insisted that we come in and partake of such as she had, telling us
that she had very little left, as the commissary from Atlanta had visited her and taken all the corn she had, except five barrels, which in Georgia, means twenty-five bushels. This, she and her two daughters had made with their own hands, her husband being in the Virginia army. She then told us about this man at the big, white house, who had never been in the army, but had an exemption on pretense of working in a saltpetre cave and had never had any forage taken by the commissary from Atlanta, as he had protection papers, so she called them, from his general at Atlanta. I merely mention these cases to show you the condition at that time, of the State of Georgia, the worthy people submitting patriotically to all manner of abuse by some of our army officials, while some of the rich, through nefarious practices, escaped the weight of war. Thanking this lady for her kind offer, which we could not afford to accept, we continued on this road and two miles further on struck a large cornfield with tempting roasting ears and decided to stop, build a fire, dry our clothes and roast corn for our meal, feeding our horses on the same, in moderation. We had to build our fire of rails taken off the fence and very soon were enjoying our roasting ears and the warm fire, being somewhat chilled by the rain. The proprietor of the place came up the road and, judging from his manner and looks, was pretty mad, when he said, “Gentlemen, if you had come to the house I would have gladly given you a good meal and fed your horses, rather than to see the destruction of my rails.” I told him that we didn’t believe it, that we had tried several places up on the road and were refused because we had no money and he, no doubt, noting that we were in no mood for argument, decided that he had better say no more. We then proceeded on our road to Covington. When on our arrival there we found that Wheeler, with all the cavalry having horses fit for service, had gone on a raid into Middle Tennessee, by way of Dalton, tearing up the railroad in Sherman’s rear for many miles, and finally entering Middle Tennessee, returning by way of Mussels Shoals, rejoining the army below Atlanta.
After the battle of Jonesboro, Hood started on his fatal Middle Tennessee campaign, his march to the Tennessee River being covered by our cavalry, making a feint at Rome, Georgia, to which point General Sherman had followed, confidently expecting to give
Hood battle at Gadsden and never suspecting his move towards the Tennessee River. While concentrating his army at Rome, Harrison’s Brigade, under Colonel Harrison, commanding our regiment, made a feint on Rome by dismounting, hiding our horses in the rear in the woods, out of sight, and advanced on the outer works of Rome, preceded by a line of skirmishers. For this purpose, not having our battle flag with us, we used a new flag, sent us from Nashville, made by a couple of young ladies from their silk dresses, with the name of Terry’s Texas Rangers worked in gold letters and some Latin words on the other side. After skirmishing with Sherman’s infantry a short time, we retired down the valley, which at this point was perhaps a couple of miles wide, from the hills to the bottoms.
Falling back that night some six or eight miles, we struck a wooded ridge, running from the hills to the bottom, perhaps nearly three miles long. This ridge overlooked the country in front towards Rome, several miles. General Sherman coming out in person with a corps of his infantry, expecting to give Hood battle the next morning, discovered there was only a handful of cavalry in his front, which was Harrison’s Brigade, and which he was specially anxious to capture. For this purpose he sent a heavy cavalry force, perhaps three times our number, into our rear, flanking our position by moving through the hills on our left, then occupying nearly every road in our rear, for eight or ten miles. During the night we received reinforcements of Pillow’s Brigade, a new command, which had been in only one engagement, at La Fayette, Georgia, where they were badly handled, causing the loss of a great many killed and wounded and in consequence, they were a little demoralized. We also received a section of artillery, two pieces, under a lieutenant, whose name I do not remember.
This artillery was stationed on a hill to the left of our position, under an old gin house.
Immediately after taking position the artillery opened on the enemy, a heavy line of battle making its appearance in the edge of the woods, about a mile distant. The Rangers were kept mounted, drawn up near this old gin house, supporting the battery, when all the
rest of the two brigades had been dismounted with their horses immediately in the rear, out of sight of the enemy.
Very soon a courier from the right of our line, dashed up to Colonel Harrison and reported that the enemy were flanking us, down in the bottom, with a heavy force. Harrison abused him, told him to go back and tell his colonel if he sent him another such message he would have him court martialed, but very soon a lieutenant dashed up from the extreme right of our line, reporting the enemy advancing in the bottom, and about to outflank us, when Colonel Harrison decided to ride down in the rear of our line and ascertain conditions for himself. Immediately the enemy raised a shout and charged. The lieutenant of the battery, concluding that his guns were in danger of being captured, limbered up and ran down to the road, where he met Colonel Harrison returning and was by him ordered to unlimber and open again on the enemy, when he succeeded in firing one shot and was sabered right over his guns by the enemy’s cavalry. In the meantime, through some misapprehension of orders, the Alabama Brigade broke for their horses, followed by the balance of our brigade, when our regiment was ordered to charge their cavalry, which we did, striking them on their flank, using our six-shooters, to which they paid no attention, simply calling out, “Clear the road for the Fourth Regulars!” This Fourth Regulars was commanded by a Captain McIntyre from Brenham, Texas, who was in the United States Army, a lieutenant, when the war broke out, having just graduated at West Point.
It is hardly necessary to say that finding the enemy’s cavalry in our rear for a great many miles, resulted in a general stampede, everybody trying to make their escape out of it. In recording this engagement I regret to have to mention the loss of our beautiful flag which, encased in a rubber cover, slipped off its staff and was found by a Major Weiler, commanding a battalion of the Seventeenth Mounted Indiana Infantry, and after many years, returned to us at Dallas, Texas, by Governor Mount and staff, instructed to do so by a joint resolution of the Indiana Legislature, in response to a memorial, drawn up and sent by me.
In this engagement the Terry Rangers lost no prisoners, had only a few wounded and none killed, while the Alabamians’ loss was quite heavy in prisoners and the balance of Harrison’s Brigade had very few men taken prisoners. I made my escape by crossing the big road, being joined by about eight or ten Alabamians, one of whom was shot in the fleshy part of the thigh, which somewhat demoralized him, when he called on me, “Texas, can you take us out of here?” I told him, “Yes, follow me; I’ll take you out.” I struck out straight for the river bottom, the Federal cavalry not following us, and when out of sight of the main road, in a little branch bottom, I called a halt and told the men my plan of trying to swim the river, as the road ahead of us seemed to be occupied for many miles, judging by the scattered firing a great distance ahead of us. The wounded man straightened up in the saddle and asked me if I was an officer. I told him, “No,” and he said that he was a lieutenant and would take command of the squad. I told him he could take command of his own men, but he couldn’t command me, and told his men, “Now, all of you boys that want to go out with me, come on,” when they all followed me, including the lieutenant.
Reaching the high ground on the other side of the branch, I discovered a house, with a lone cavalry-man at the front gate, and, getting a little nearer, I recognized him as one Joe Harris, of our company, who was well acquainted in that section, having married, near Cedartown, the daughter of a Doctor Richardson, just on the other side of the river. He suggested to me that he knew of a batteau about seven miles this side of Rome; that we go up there, put our saddles and equipments into the boat, swim our horses across, then go to Doctor Richardson and get a good dinner; to which I, of course, readily consented. On our way to this batteau, following the river in the bottom, we struck hundreds of Alabamians trying to find a crossing place. These men we took along with us and when we reached the boat we were the first ones to cross, leaving the Alabamians there to cross as fast as they were able. Joe and I then rode to Doctor Richardson’s, about ten or fifteen miles, and by three o’clock sat down to a sumptuous dinner Here we stayed all night and the next morning recrossed the river, finally striking the main Gadsden road and finding our stampeded forces gathering at some
gap, the name of which I have forgotten. Here we met General Wheeler, with the balance of his command. We then moved down to the town of Gadsden, where we recrossed the river and spent several days resting our horses and ourselves.
General Hood, in the meantime, with his army, crossed the Tennessee River, and General Sherman returned to Atlanta, leaving Thomas’ Corps to follow Hood into Middle Tennessee. Wheeler and his cavalry returned to below Atlanta, where we struck Sherman’s forces moving in the direction of Macon, Georgia, by way of Augusta to Savannah. We then had daily engagements with Kilpatrick’s cavalry, often driving them into their infantry. Sherman used his cavalry to forage for the army, depending altogether on the country for his commissary. To enter into detail of the many engagements had on this trip would occupy too much time and space. Our service was largely, as stated, to keep his cavalry from foraging, burning and destroying the country. In connection with this I would mention an incident at Macon:
I was at a blacksmith’s shop with a comrade by the name of Freeman, who was about seven years my senior in age. While waiting to get our horses shod we heard artillery, supported by small arms, open at our works, about a mile across the river. We immediately mounted our horses and dashed over there and just as we got in sight of the roadway through the breastworks we witnessed a lone trooper of Kilpatrick’s cavalry coming up the road through the works, having his horse shot just as he reached inside. His horse fell on his leg, from which position he was trying to extricate himself and was about to be shot by an excited militia of young and old men, who had never been under fire before, when Jim put spurs to his horse and with his pistol raised, dashed up to where this man lay under his horse, and drove off the excited militia, I, of course, following him. He called up a lieutenant, asked his name, company and regiment; told him to take charge of that prisoner and see that he was well treated, that he would hold him personally responsible for his safety, and immediately wheeled his horse, I following him, and returned to town without giving the lieutenant a chance to ask questions. On our return I asked Jim Freeman his reasons for doing as he did, risking
