04 December 2023: Articles
A Case Report of a Rare ER+, PR- Pure Metaplastic Breast Squamous Cell Carcinoma with HER2 Overexpression
Challenging differential diagnosis, Unusual or unexpected effect of treatment, Rare disease
Shafawati Akmal Adam1ABCDEF, Khairatul Nainey Kamaruddin1E, Nordashima Abd Shukor2BCDEF, Shahrun Niza Abdullah Suhaimi3CDE, Fuad Ismail4CDE, Mazapuspavina Md Yasin 1ABCDEF*DOI: 10.12659/AJCR.941448
Am J Case Rep 2023; 24:e941448
Abstract
BACKGROUND: Breast squamous cell carcinoma (SCC) is a subtype of metaplastic breast carcinoma (MBC), which is a rare malignancy and accounts for 0.1% of all invasive breast carcinomas. Guidelines on definitive management and treatment of breast SCC are not well established, given its rarity and diverse immunohistochemistry (IHC) profile, and lack of clinical data. Most cases of breast SCC are triple-negative breast cancer – negative for estrogen receptor (ER), progesterone receptor (PR), and human epidermal growth factor receptor 2 (HER2). This case report outlines the clinicopathological profile of a pure breast SCC case with a rare IHC profile; HER2 and ER positive.
CASE REPORT: A 41-year-old woman presented with a right breast mass that had been growing for 2 months. Biopsy confirmed breast SCC, a rare malignancy with IHC profile as follows: HER2 overexpression, ER positive, and PR negative. She underwent neoadjuvant chemotherapy for 3 months followed by right mastectomy with axillary clearance, adjuvant radiotherapy, and oral tamoxifen therapy. Unfortunately, she did not receive anti-HER2 therapy. She developed early locoregional recurrence at 2 months postoperatively, which was treated with excision of the right chest wall and transverse rectus abdominis musculocutaneous (TRAM) flap. She developed liver and lung metastasis and succumbed to her disease at 15 months post-diagnosis.
CONCLUSIONS: Breast SCC is a rare and aggressive tumor with heterogeneous clinicopathological features. Available guidelines do not outline the definitive treatment for breast SCC, given its rarity and heterogenous IHC profile, leading to a general lack of clinical data. Hence, due to the challenges in managing this rare condition, treatment modalities need to be individualized.
Keywords: Breast Neoplasms, Carcinoma, Metaplasia, Neoplasms, Squamous Cell, Female, Humans, Adult, Receptors, Estrogen, Receptors, Progesterone, Mastectomy, Carcinoma, Squamous Cell, Triple Negative Breast Neoplasms
Background
Metaplastic breast carcinoma (MBC) is a rare malignancy that accounts for 0.1% of all invasive breast carcinomas [1]. It is categorized into 5 subtypes - squamous cell carcinoma (SCC), spindle cell carcinoma, matrix-producing carcinoma, carcinosarcoma, and metaplastic carcinoma with osteoclastic giant cells [2].
Breast SCC is further classified into mixed or pure SCC depending on the presence or absence of adenocarcinoma components. Pure or monophasic breast SCC predominates, with more than 90% squamous cells, and it tends to be more aggressive and refractory to treatment [3]. Primary pure SCC is diagnosed when (a) there is a clear predominance (>90% of areas with SCC) at the histologic examination, (b) the tumor is independent of the overlying skin, and (c) other primary SCC sites are excluded [4].
The knowledge of clinicopathological features, radiological characteristics, optimal treatment course, and prognosis is still controversial and not well understood given its rare prevalence. Generally, it is believed that most cases of primary pure SCC are triple-negative breast cancer – negative for estrogen receptor (ER), progesterone receptor (PR), and human epidermal growth factor receptor 2 (HER2), and thus hormonal targeted therapies are unfortunately ineffective as treatments [5]. Given its rarity and heterogeneous immunohistochemical (IHC) profile, there is a paucity of clinical evidence and therefore no defined guidelines for the treatment of breast SCC. The majority of treatment and management approaches for classical breast cancer include surgery, chemotherapy, and radio-therapy [6]. Breast SCC with HER2 overexpression is rare. Lei et al have reported only 2 cases with HER2 overexpression [5]. Here, we will present a case of this rare breast malignancy of breast SCC with an even rarer IHC profile: ER positive, overexpression of HER2, and PR negative.
Case Report
A 41-year-old, nulliparous, premenopausal woman with a previous history of laparotomy cystectomy for endometriosis, presented with a right breast lump that had been increasing in size for 2 months. There was no mastalgia, no overlying skin changes, no nipple retraction, no nipple discharge, and no constitutional symptoms. She had no family history of malignancies.
Physical examination revealed a 3×3 cm mass at 9 o’clock in the right breast, 2 cm from the nipple, firm and not mobile. There was no axillary lymph node palpable and the rest of the systemic examination was unremarkable.
She was referred to a tertiary center and an ultrasound of the breast showed a hemorrhagic cyst. She underwent ultra-sound-guided fine needle biopsy but it was inconclusive. She then underwent a right breast cystectomy. Pathological examination revealed SCC and the malignant cells were positive for the following squamous markers: p63 and cytokeratin 5/6 (CK5/6) (Figure 1). The IHC profile was ER: 40%, PR: negative, HER2: positive, with cellular erythroblastic oncogene B (C-erb-B2): 3+ amplified (Figure 2). In addition, programmed death ligand-1 (PDL-1) was negative.
She underwent a diagnostic mammogram which showed heterogenous fibroglandular density with a large mass and multiple smaller high-density lesions in the right upper quadrant. No microcalcifications were seen (Figure 3A). Complementary ultrasound revealed a large thick-walled lobulated cystic mass measuring 2.7×3.4×3.4 cm with septations (Figure 3B) and an enlarged right axillary node with a cystic area measuring 1.2 cm in short axis diameter (Figure 3C). A computed tomography scan of the neck, thorax, abdomen, and pelvis (CT-TAP) was done and ruled out distant metastases and other primary tumors of the squamous cell carcinoma. Therefore, a definite diagnosis of primary SCC of the breast was confirmed. The clinical staging at this point was cT2N1M0 (T: tumor; N: nodes; M: metastasis), which indicated that the carcinoma was stage group IIB.
Given the large mass, the patient underwent neoadjuvant chemotherapy for 3 cycles of 3X-weekly paclitaxel plus carboplatin. However, little response was seen. The patient subsequently underwent a right mastectomy and axillary clearance. Pathology confirmed a residual pure metaplastic SCC with therapy effect seen and a single nodal involvement. Post-operative staging was ypT3 ypN1mi (yp: post-treatment findings; mi: microscopic), which is equivalent to stage IIIB.
Next, she was scheduled for a course of radiotherapy of 22 Gy to the chest wall, but midway through treatment, she developed local recurrence over the right chest wall which was confirmed by biopsy. This was 2 months postoperatively and 5 months post-diagnosis. The radiotherapy was stopped after 11 fractions, and she underwent an excision of the right chest wall recurrence and transverse rectus abdominis musculocutaneous (TRAM) flap.
One month after excision of the right chest wall and TRAM flap, she underwent a second course of radiotherapy with a dose of 61.2 Gy in 26 fractions. Unfortunately, she developed more suspicious nodules over the right chest wall region and boost radiotherapy was given with a dose of 22 Gy in 10 fractions. Radiotherapy was complicated by localized grade 3 moist desquamation of the chest wall.
She eventually developed metastatic disease 9 months postoperatively and 12 months post-diagnosis. CT-TAP showed a right pleural collection with thickened heterogeneous enhancing pleura and adjacent right rib erosions, irregular liver margin with ill-defined hypodense lesions suggestive of liver infiltration and lung metastasis as evidenced by multiple left lung nodules, with cavitation at the left lower lobe.
She was given 3 cycles of palliative chemotherapy consisting of gemcitabine and cisplatin, and this provided minor symptom relief, but her overall condition continued to deteriorate. Given that her tumor was ER positive with HER2 overexpression, she was also given hormonal targeted therapy; namely, oral tamoxifen, but not anti-HER2 such as trastuzumab and pertuzumab. However, the cancer continued to progress and she eventually succumbed to her disease, 12 months postoperatively and 15 months post-diagnosis.
Discussion
MBC is a rare malignancy and accounts for 0.1% of all invasive breast carcinomas [1]. Breast SCC is a subtype of MBC that is mostly triple negative [5]. The present case report aimed to describe the clinicopathological features of a rare SCC breast malignancy that carried an even rarer IHC profile: ER positive, PR negative, and with HER2 overexpression.
Breast SCC is more common in older women, mostly postmenopausal. One study reported occurrence in women between the ages of 26 and 99 years old, and found a median age at diagnosis of 67 years old [7]. It usually presents as a rapidly growing breast mass with an average size upon presentation of 5 cm but can range from 2 to 16 cm. Other reported associated symptoms include breast pain or inflammation, nipple discharge or retraction, sometimes ulceration of the skin or breast abscess, and less frequently, axillary lymph node involvement [8,9]. The most common stage at presentation is Stage II [7,8]. In contrast, our patient was diagnosed at the age of 41 years, she was premenopausal, and there was one instance of axillary lymph node involvement during presentation. Although she presented with a typical rapidly growing breast mass, she had no other associated symptoms. Our patient was also at stage IIB upon presentation. Meanwhile, the patients with HER2 overexpression reported by Lei et al were 54 and 43 years old. They presented earlier, within around 7 to 10 days of noticing the breast lump, with lump size during presentation of 2×2 cm and 3×2 cm, respectively. Both cases did not have axillary lymph node enlargement during presentation [5].
The radiological appearances of breast SCC is often nonspecific. It may appear as a rounded or irregular mass, with high density on mammography and microlobulated appearance on sonography, with complex echogenicity reflecting solid and cystic components owing to the presence of cystic and necrotic degeneration [10]. There is a general lack of spicules or microcalcifications in breast SCC [10] but some reports have noted the presence of these features [9,11]. Radiological findings, in our case, showed a dense, microlobulated cystic mass without microcalcifications. Meanwhile, both cases reported by Lei et al featured irregular-shaped masses, which had similar hypoechoic lesions with internal heterogeneous echogenicity [5].
About 93% of breast SCC cases show a triple-negative profile (ER-, PR-, and HER2-negative), and are positive for high molecular weight cytokeratins such as CK5/6 (seen in 75% of cases) and p63 (seen in 70% of cases) [12]. ER and PR are hormonal receptors that are attached to human reproductive cells, including normal and cancerous breast cells, that help them grow, while HER2 is a receptor that may be attached to tumor cells, and responds to HER2 protein to help them grow. Knowing this status helps the clinician to understand more about the tumor profile and may determine the treatment options. On the other hand, CK5/6 and p63 are markers associated with squamous cell carcinoma [12].
To date, only 6 cases of breast SCC with HER2 overexpression have been reported; 1 was HER2 positive, PR positive, and ER negative [13], while the other 5 were HER2 positive, ER negative, and PR negative [5,14]. Among these 6 cases, the 2 reported by Lei et al had tumor cells that were positive for p63 and CK 5/6, had HER2 overexpression, and were negative for ER and PR [5]. Our case is the only reported case of a HER2-positive, ER-positive, and PR-negative SCC. Specifically, the tumor was 40% ER positive and PR negative, and it showed HER2 overexpression with cellular erythroblastic oncogene B (c-erb-B2) expression at 3 times the normal level. The tumor was also positive for CK5/6 and p63, indicating its squamous cell origin.
There are no standardized guidelines on definitive treatment for breast SCC given the lack of clinical data on this carcinoma due to its rarity and heterogenous IHC profile. Management plans mostly adopt classical techniques for breast cancer management, consisting of surgery, chemotherapy, and radiotherapy [6]. Given its known aggressive behavior, upfront mastectomy with axillary clearance is the mainstream treatment, since most cases have nodal involvement [15]. It was previously believed that there was no role for neoadjuvant chemotherapy in breast SCC [16]. Nonetheless, if the tumor size is inoperable, neoadjuvant chemotherapy may play a role in shrinking its size as there have been reports of cases with good response [17]. In our case, the patient underwent neoadjuvant chemotherapy and, subsequently, surgical resection. The tumor was then staged based on the American Joint Committee on Cancer (AJCC) 8th Edition with Tumor, Node, Metastasis (TNM) staging. We used ypTNM classification, which describes the extent of the tumor after exposure to neoadjuvant therapy [18]. The postoperative staging was ypT3 ypN1mi, and histopathology examination revealed an extensive tumor burden despite the patient having received neoadjuvant therapy; the tumor showed little response to the therapy. Meanwhile, both cases reported by Lei et al did not receive any neoadjuvant therapy, given the small size of the mass, and both patients received radical surgery of the affected breast with axillary clearance; each of the cases had a 2-cm mass of tumor removed [5].
Contradictory evidence is also seen in the role of adjuvant chemotherapy and radiotherapy in managing this disease. Though there is not much evidence on the role of adjuvant radiotherapy in breast SCC, it might be useful as the response has been seen in SCC of other sites [11]. However, locoregional relapse is frequently seen within the irradiated field [16]. On the other hand, resistance to chemotherapy may be attributed to its complex genetic and nongenetic makeup. Hence, the disease-free survival rate is poor [3]. Similarly, in our case, the tumor showed its aggressive behavior as the patient developed local recurrence over the chest wall within 3 months postoperatively while receiving adjuvant radiotherapy, and she developed distant metastasis involving the lung and liver at 9 months postoperatively. Meanwhile, the first case of a patient with a tumor with HER2 overexpression reported by Lei et al did not receive any adjuvant therapy and remained disease-free for 34 months postoperatively. On the other hand, in the second case reported by Lei et al, the patient had postoperative adjuvant therapy but the author did not specify whether it was chemotherapy or radiotherapy. The case was unfortunately complicated by lung metastasis that was found 14 months postoperatively [5].
Targeted hormonal therapies seem to have no role in SCC breast carcinoma treatment, as most SCC breast patients are triple negative. However, there might be a role for targeted hormonal therapies in patients with hormone receptor-positive tumors, but given the rarity of these types of tumors, more clinical data are needed to decide on the best treatment options [5]. Our patient was started on oral tamoxifen, a selective estrogen receptor modulator. Anti-HER2 works as an anti-cancer agent by binding to the HER2 receptor and blocking its pairing with other HER receptors [5]. Although our patient showed overexpression of HER2, she was not started on anti-HER2 by the treating oncology team. Similarly, both cases reported by Lei et al did not receive anti-HER2 as the patient refused, despite having HER2 overexpression [5].
Besides targeted hormonal therapy, there are updates on the role of immunotherapy. Immunotherapy acts to harness the patient’s immune system in attacking cancer cells. PDL-1 is a protein molecule that is found on the surface of various cells, including cancer cells, as well as normal cells, particularly immune cells, including neutrophils, macrophages, dendritic cells, natural killer cells, mast cells, T lymphocytes, B lymphocytes, plasma cells, and memory cells. The mechanism of the therapy is to modulate the immune reaction towards antigens. The use of an inhibitor (anti-PDL-1) blocks the interaction of PDL-1 with the programmed death-1 (PD-1) receptor, thereby preventing cancer cells from evading the immune system [11]. However, there was no role for anti-PDL-1 in our patient as her tumor was PDL-1 negative. Lei et al did not mention the status of PDL-1 for either of the cases that they reported [5].
Breast SCC is very aggressive and has a poor prognosis, with a 5-year overall survival of 62.1% [19]. Poorer prognosis has been associated with having a larger tumor (larger than 3 cm), having nodal involvement, and the patient being a women below the age of 40 years old [15,20]. In our case, the tumor size was more than 3 cm, with 1 nodal involvement, and the patient’s age was 41 years old upon presentation. Unfortunately, our patient succumbed to death after 15 months following diagnosis. Both of the cases reported by Lei et al presented when the tumor size was 2 cm with nodal involvement in 1 of the cases. The first patient presented at an older age, 54 years, and had a better outcome; she remained disease-free at 34 months postoperatively. The second patient presented at 43 years of age, and developed lung metastasis at 14 months postoperatively [5].
Assessment, diagnosis, and management for this patient were conducted in adherence to the Malaysian Clinical Practice Guidelines on Management of Breast Cancer, 3rd edition, 2019. It was recommended for diagnosis that the patient undergo a minimally invasive biopsy technique (MIBT) with a core needle, followed by surgical excision as the initial core biopsy result was non-diagnostic. The estrogen, progesterone, and HER2 receptor status was examined. The HER2 gene status was validated using dual color silver in situ hybridization. Further imaging investigations for metastasis were performed to assess the extent of the disease. It is advocated that management utilizes a multidisciplinary team approach. Neoadjuvant chemotherapy was given to enable breast-conserving surgery. However, she was not responding well to it, thus requiring a mastectomy with axillary clearance. Adjuvant radiotherapy was given postmastectomy. Adjuvant extended endocrine therapy (tamoxifen) was given as she had ER-positive breast cancer. The guidelines recommend trastuzumab-based therapy for patients with HER2-positive breast cancer, and the addition of pertuzumab as a dual HER2 blockade may be considered in high-risk patients, but unfortunately this was not given due to personal reasons [21].
From a primary care physician (PCP) point of view, PCPs are the usual initial point of contact as patients frequently go to a PCP for consultations on new health complaints. Awareness of the aggressive behavior of this rare disease, its clinical profile, along with the poor prognostic factor of being a young patient is important for PCPs. It is salient that PCPs have a high index of suspicion and act promptly, thus avoiding delays in referral to the tertiary center for further urgent management. This case also highlights the importance of multidisciplinary team involvement and the importance of each specialty in managing the disease from the time of the first encounter until the last followup.
Conclusions
Breast SCC is an aggressive tumor with heterogeneous clinico-pathological features. The Malaysian Clinical Practice Guidelines for Breast Cancer Management does not specifically outline the management of breast SCC. In addition, as revealed by the authors’ updated literature searches, there are no international guidelines specifically for breast SCC. Therefore, treatment needs to be individualized based on the IHC profiles. There may be hope for this rare disease group with non-triple negative breast cancer as there is emerging evidence on targeted hormonal and immunotherapy. Given the heterogeneity of this disease, more clinical data need to be gathered to determine the benefit and effectiveness of each therapeutic modality in managing the disease to improve patient survival. Though our patient did not survive, reporting her case, which was characterized by a unique clinicopathological and IHC profile, adds to the clinical data on breast SCC.
Figures
Figure 1.. (A, B) Histopathological slides from cyst wall curettage. The image shows multiple fragments of fibro-collagenous tissue infiltrated by malignant squamous cells arranged in trabeculae, nests, and singly distributed surrounded by desmoplastic stroma. The malignant cells are enlarged, polygonal, and moderately to markedly pleomorphic, displaying hyperchromatic nuclei, some with prominent nucleoli and ample eosinophilic cytoplasm. Mitosis is frequently seen. Dyskeratotic cells and focal intercellular bridges are present. No keratin pearl formation was noted. No lymphovascular invasion was seen. The background shows blood and some foamy macrophages. Hematoxylin & Eosin (H&E): 200× and 400× magnification. (C, D) The malignant cells are positive for squamous markers: (C) strong membrane/cytoplasmic staining for CK5/6, and (D) mild to moderate nuclear staining for the p63 tumor protein (400X magnification). Figure 2.. (A, B) Immunohistochemistry (IHC) of the cyst wall curettage. (A) IHC shows that malignant cells are positive for estrogen receptors with 40% positivity of moderate to strong intensity. (B) IHC shows strong expression (3+) for erythroblastic oncogene B-2 (c-erb-B2). (400× magnification) Progesterone receptor: negative. Figure 3.. (A) Right breast mammogram. (B) Ultrasound of the right breast. (C) Ultrasound of the right axillary lymph node. (A) Right breast mammogram showing heterogenous fibro glandular density. The Breast imaging reporting and data system (BIRADS) level was C, showing a large mass at the right upper quadrant. Multiple smaller high-density lesions in the right upper quadrant of the breast are visible. An area of hyperdensity over the right breast, upper quadrant, is visible. The red arrows show a dense, microlobulated cystic mass (these are typical mammography findings prompting suspicion of breast cancer). There is an associated right breast diffuse opacity due to edema. No suspicious grouped microcalcifications were seen. (B) Large thick-walled lobulated cystic mass with septations occupying the right upper quadrant, measuring 2.7×3.4×3.4 cm. There was a linear hypoechogenicity across the anterior aspect of the lesion in keeping with the previous wound. Several ill-defined hypoechoic lesions at the medial aspect of the above-mentioned lesions were visible. They were increased in size and number compared with recent sonograms, at the 12 o’clock and 1 o’clock positions; ranging from 0.7 cm to 2.3 cm. The overlying skin appeared to be thickened. (C) Enlarged right axillary node with cystic area measuring 1.2 cm in short axis diameter.References:
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